Nonlytic cellular release of hepatitis A virus requires dual capsid recruitment of the ESCRT-associated Bro1 domain proteins HD-PTP and ALIX Article Swipe
Takayoshi Shirasaki
,
Hui Feng
,
Helen M. E. Duyvesteyn
,
William G. Fusco
,
Kevin L. McKnight
,
Ling Xie
,
Mark S. Boyce
,
Prashant Kumar
,
Rina Barouch‐Bentov
,
Olga González‐López
,
Ryan P. McNamara
,
Li Wang
,
Adriana Hertel-Wulff
,
Xian Chen
,
Shirit Einav
,
Joseph A. Duncan
,
Maryna Kapustina
,
Elizabeth E. Fry
,
David I. Stuart
,
Stanley M. Lemon
·
YOU?
·
· 2022
· Open Access
·
· DOI: https://doi.org/10.17615/cc9h-0b78
YOU?
·
· 2022
· Open Access
·
· DOI: https://doi.org/10.17615/cc9h-0b78
Although picornaviruses are conventionally considered ‘nonenveloped’, members of multiple picornaviral genera are released nonlytically from infected cells in extracellular vesicles. The mechanisms underlying this process are poorly understood. Here, we describe interactions of the hepatitis A virus (HAV) capsid with components of host endosomal sorting complexes required for transport (ESCRT) that play an essential role in release. We show release of quasi-enveloped virus (eHAV) in exosome-like vesicles requires a conserved export signal located within the 8 kDa C-terminal VP1 pX extension that functions in a manner analogous to late domains of canonical enveloped viruses. Fusing pX to a self-assembling engineered protein nanocage (EPN-pX) resulted in its ESCRT-dependent release in extracellular vesicles. Mutational analysis identified a 24 amino acid peptide sequence located within the center of pX that was both necessary and sufficient for nanocage release. Deleting a YxxL motif within this sequence ablated eHAV release, resulting in virus accumulating intracellularly. The pX export signal is conserved in non-human hepatoviruses from a wide range of mammalian species, and functional in pX sequences from bat hepatoviruses when fused to the nanocage protein, suggesting these viruses are released as quasi-enveloped virions. Quantitative proteomics identified multiple ESCRT-related proteins associating with EPN-pX, including ALG2-interacting protein X (ALIX), and its paralog, tyrosine-protein phosphatase non-receptor type 23 (HD-PTP), a second Bro1 domain protein linked to sorting of ubiquitylated cargo into multivesicular endosomes. RNAi-mediated depletion of either Bro1 domain protein impeded eHAV release. Super-resolution fluorescence microscopy demonstrated colocalization of viral capsids with endogenous ALIX and HD-PTP. Co-immunoprecipitation assays using biotin-tagged peptides and recombinant proteins revealed pX interacts directly through the export signal with N-terminal Bro1 domains of both HD-PTP and ALIX. Our study identifies an exceptionally potent viral export signal mediating extracellular release of virus-sized protein assemblies and shows release requires non-redundant activities of both HD-PTP and ALIX.
Related Topics
Concepts
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.17615/cc9h-0b78
- OA Status
- green
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4294367720
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W4294367720Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.17615/cc9h-0b78Digital Object Identifier
- Title
-
Nonlytic cellular release of hepatitis A virus requires dual capsid recruitment of the ESCRT-associated Bro1 domain proteins HD-PTP and ALIXWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2022Year of publication
- Publication date
-
2022-09-03Full publication date if available
- Authors
-
Takayoshi Shirasaki, Hui Feng, Helen M. E. Duyvesteyn, William G. Fusco, Kevin L. McKnight, Ling Xie, Mark S. Boyce, Prashant Kumar, Rina Barouch‐Bentov, Olga González‐López, Ryan P. McNamara, Li Wang, Adriana Hertel-Wulff, Xian Chen, Shirit Einav, Joseph A. Duncan, Maryna Kapustina, Elizabeth E. Fry, David I. Stuart, Stanley M. LemonList of authors in order
- Landing page
-
https://doi.org/10.17615/cc9h-0b78Publisher landing page
- Open access
-
YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
- OA URL
-
https://doi.org/10.17615/cc9h-0b78Direct OA link when available
- Concepts
-
Capsid, ESCRT, Endosome, Virology, Cell biology, Domain (mathematical analysis), Chemistry, Virus, Biology, Computational biology, Intracellular, Mathematical analysis, MathematicsTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
0Total citation count in OpenAlex
- Related works (count)
-
10Other works algorithmically related by OpenAlex
Full payload
| id | https://openalex.org/W4294367720 |
|---|---|
| doi | https://doi.org/10.17615/cc9h-0b78 |
| ids.doi | https://doi.org/10.17615/cc9h-0b78 |
| ids.openalex | https://openalex.org/W4294367720 |
| fwci | 0.0 |
| type | article |
| title | Nonlytic cellular release of hepatitis A virus requires dual capsid recruitment of the ESCRT-associated Bro1 domain proteins HD-PTP and ALIX |
| biblio.issue | |
| biblio.volume | |
| biblio.last_page | |
| biblio.first_page | |
| topics[0].id | https://openalex.org/T12025 |
| topics[0].field.id | https://openalex.org/fields/27 |
| topics[0].field.display_name | Medicine |
| topics[0].score | 0.9994000196456909 |
| topics[0].domain.id | https://openalex.org/domains/4 |
| topics[0].domain.display_name | Health Sciences |
| topics[0].subfield.id | https://openalex.org/subfields/2721 |
| topics[0].subfield.display_name | Hepatology |
| topics[0].display_name | Hepatitis Viruses Studies and Epidemiology |
| topics[1].id | https://openalex.org/T10151 |
| topics[1].field.id | https://openalex.org/fields/27 |
| topics[1].field.display_name | Medicine |
| topics[1].score | 0.992900013923645 |
| topics[1].domain.id | https://openalex.org/domains/4 |
| topics[1].domain.display_name | Health Sciences |
| topics[1].subfield.id | https://openalex.org/subfields/2721 |
| topics[1].subfield.display_name | Hepatology |
| topics[1].display_name | Hepatitis C virus research |
| topics[2].id | https://openalex.org/T11834 |
| topics[2].field.id | https://openalex.org/fields/27 |
| topics[2].field.display_name | Medicine |
| topics[2].score | 0.9811999797821045 |
| topics[2].domain.id | https://openalex.org/domains/4 |
| topics[2].domain.display_name | Health Sciences |
| topics[2].subfield.id | https://openalex.org/subfields/2721 |
| topics[2].subfield.display_name | Hepatology |
| topics[2].display_name | Liver Diseases and Immunity |
| is_xpac | False |
| apc_list | |
| apc_paid | |
| concepts[0].id | https://openalex.org/C202878990 |
| concepts[0].level | 3 |
| concepts[0].score | 0.9077016711235046 |
| concepts[0].wikidata | https://www.wikidata.org/wiki/Q830465 |
| concepts[0].display_name | Capsid |
| concepts[1].id | https://openalex.org/C143876685 |
| concepts[1].level | 4 |
| concepts[1].score | 0.8775248527526855 |
| concepts[1].wikidata | https://www.wikidata.org/wiki/Q22327705 |
| concepts[1].display_name | ESCRT |
| concepts[2].id | https://openalex.org/C102747710 |
| concepts[2].level | 3 |
| concepts[2].score | 0.6239606142044067 |
| concepts[2].wikidata | https://www.wikidata.org/wiki/Q824237 |
| concepts[2].display_name | Endosome |
| concepts[3].id | https://openalex.org/C159047783 |
| concepts[3].level | 1 |
| concepts[3].score | 0.4997854232788086 |
| concepts[3].wikidata | https://www.wikidata.org/wiki/Q7215 |
| concepts[3].display_name | Virology |
| concepts[4].id | https://openalex.org/C95444343 |
| concepts[4].level | 1 |
| concepts[4].score | 0.4933585226535797 |
| concepts[4].wikidata | https://www.wikidata.org/wiki/Q7141 |
| concepts[4].display_name | Cell biology |
| concepts[5].id | https://openalex.org/C36503486 |
| concepts[5].level | 2 |
| concepts[5].score | 0.4671674966812134 |
| concepts[5].wikidata | https://www.wikidata.org/wiki/Q11235244 |
| concepts[5].display_name | Domain (mathematical analysis) |
| concepts[6].id | https://openalex.org/C185592680 |
| concepts[6].level | 0 |
| concepts[6].score | 0.45932361483573914 |
| concepts[6].wikidata | https://www.wikidata.org/wiki/Q2329 |
| concepts[6].display_name | Chemistry |
| concepts[7].id | https://openalex.org/C2522874641 |
| concepts[7].level | 2 |
| concepts[7].score | 0.419036328792572 |
| concepts[7].wikidata | https://www.wikidata.org/wiki/Q808 |
| concepts[7].display_name | Virus |
| concepts[8].id | https://openalex.org/C86803240 |
| concepts[8].level | 0 |
| concepts[8].score | 0.36846140027046204 |
| concepts[8].wikidata | https://www.wikidata.org/wiki/Q420 |
| concepts[8].display_name | Biology |
| concepts[9].id | https://openalex.org/C70721500 |
| concepts[9].level | 1 |
| concepts[9].score | 0.3446241319179535 |
| concepts[9].wikidata | https://www.wikidata.org/wiki/Q177005 |
| concepts[9].display_name | Computational biology |
| concepts[10].id | https://openalex.org/C79879829 |
| concepts[10].level | 2 |
| concepts[10].score | 0.0 |
| concepts[10].wikidata | https://www.wikidata.org/wiki/Q5571762 |
| concepts[10].display_name | Intracellular |
| concepts[11].id | https://openalex.org/C134306372 |
| concepts[11].level | 1 |
| concepts[11].score | 0.0 |
| concepts[11].wikidata | https://www.wikidata.org/wiki/Q7754 |
| concepts[11].display_name | Mathematical analysis |
| concepts[12].id | https://openalex.org/C33923547 |
| concepts[12].level | 0 |
| concepts[12].score | 0.0 |
| concepts[12].wikidata | https://www.wikidata.org/wiki/Q395 |
| concepts[12].display_name | Mathematics |
| keywords[0].id | https://openalex.org/keywords/capsid |
| keywords[0].score | 0.9077016711235046 |
| keywords[0].display_name | Capsid |
| keywords[1].id | https://openalex.org/keywords/escrt |
| keywords[1].score | 0.8775248527526855 |
| keywords[1].display_name | ESCRT |
| keywords[2].id | https://openalex.org/keywords/endosome |
| keywords[2].score | 0.6239606142044067 |
| keywords[2].display_name | Endosome |
| keywords[3].id | https://openalex.org/keywords/virology |
| keywords[3].score | 0.4997854232788086 |
| keywords[3].display_name | Virology |
| keywords[4].id | https://openalex.org/keywords/cell-biology |
| keywords[4].score | 0.4933585226535797 |
| keywords[4].display_name | Cell biology |
| keywords[5].id | https://openalex.org/keywords/domain |
| keywords[5].score | 0.4671674966812134 |
| keywords[5].display_name | Domain (mathematical analysis) |
| keywords[6].id | https://openalex.org/keywords/chemistry |
| keywords[6].score | 0.45932361483573914 |
| keywords[6].display_name | Chemistry |
| keywords[7].id | https://openalex.org/keywords/virus |
| keywords[7].score | 0.419036328792572 |
| keywords[7].display_name | Virus |
| keywords[8].id | https://openalex.org/keywords/biology |
| keywords[8].score | 0.36846140027046204 |
| keywords[8].display_name | Biology |
| keywords[9].id | https://openalex.org/keywords/computational-biology |
| keywords[9].score | 0.3446241319179535 |
| keywords[9].display_name | Computational biology |
| language | en |
| locations[0].id | doi:10.17615/cc9h-0b78 |
| locations[0].is_oa | True |
| locations[0].source.id | https://openalex.org/S7407051488 |
| locations[0].source.type | repository |
| locations[0].source.is_oa | False |
| locations[0].source.issn_l | |
| locations[0].source.is_core | False |
| locations[0].source.is_in_doaj | False |
| locations[0].source.display_name | UNC Libraries |
| locations[0].source.host_organization | |
| locations[0].source.host_organization_name | |
| locations[0].license | |
| locations[0].pdf_url | |
| locations[0].version | |
| locations[0].raw_type | article-journal |
| locations[0].license_id | |
| locations[0].is_accepted | False |
| locations[0].is_published | |
| locations[0].raw_source_name | |
| locations[0].landing_page_url | https://doi.org/10.17615/cc9h-0b78 |
| indexed_in | datacite |
| authorships[0].author.id | https://openalex.org/A5038934637 |
| authorships[0].author.orcid | https://orcid.org/0000-0001-9756-8935 |
| authorships[0].author.display_name | Takayoshi Shirasaki |
| authorships[0].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[0].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[0].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[0].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[0].institutions[0].type | healthcare |
| authorships[0].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[0].institutions[0].country_code | |
| authorships[0].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[0].author_position | first |
| authorships[0].raw_author_name | Shirasaki, Takayoshi |
| authorships[0].is_corresponding | False |
| authorships[0].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[1].author.id | https://openalex.org/A5100369169 |
| authorships[1].author.orcid | https://orcid.org/0009-0009-9597-5305 |
| authorships[1].author.display_name | Hui Feng |
| authorships[1].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[1].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[1].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[1].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[1].institutions[0].type | healthcare |
| authorships[1].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[1].institutions[0].country_code | |
| authorships[1].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[1].author_position | middle |
| authorships[1].raw_author_name | Feng, Hui |
| authorships[1].is_corresponding | False |
| authorships[1].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[2].author.id | https://openalex.org/A5018413493 |
| authorships[2].author.orcid | https://orcid.org/0000-0002-4641-5442 |
| authorships[2].author.display_name | Helen M. E. Duyvesteyn |
| authorships[2].author_position | middle |
| authorships[2].raw_author_name | Duyvesteyn, Helen M. E. |
| authorships[2].is_corresponding | False |
| authorships[3].author.id | https://openalex.org/A5029220130 |
| authorships[3].author.orcid | https://orcid.org/0009-0002-1412-4517 |
| authorships[3].author.display_name | William G. Fusco |
| authorships[3].affiliations[0].raw_affiliation_string | School of Medicine, Department of Medicine |
| authorships[3].author_position | middle |
| authorships[3].raw_author_name | Fusco, William G. |
| authorships[3].is_corresponding | False |
| authorships[3].raw_affiliation_strings | School of Medicine, Department of Medicine |
| authorships[4].author.id | https://openalex.org/A5017446710 |
| authorships[4].author.orcid | https://orcid.org/0000-0002-9099-2044 |
| authorships[4].author.display_name | Kevin L. McKnight |
| authorships[4].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[4].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[4].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[4].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[4].institutions[0].type | healthcare |
| authorships[4].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[4].institutions[0].country_code | |
| authorships[4].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[4].author_position | middle |
| authorships[4].raw_author_name | McKnight, Kevin L. |
| authorships[4].is_corresponding | False |
| authorships[4].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[5].author.id | https://openalex.org/A5100308116 |
| authorships[5].author.orcid | |
| authorships[5].author.display_name | Ling Xie |
| authorships[5].affiliations[0].raw_affiliation_string | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[5].author_position | middle |
| authorships[5].raw_author_name | Xie, Ling |
| authorships[5].is_corresponding | False |
| authorships[5].raw_affiliation_strings | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[6].author.id | https://openalex.org/A5009572636 |
| authorships[6].author.orcid | https://orcid.org/0000-0001-5811-325X |
| authorships[6].author.display_name | Mark S. Boyce |
| authorships[6].author_position | middle |
| authorships[6].raw_author_name | Boyce, Mark |
| authorships[6].is_corresponding | False |
| authorships[7].author.id | https://openalex.org/A5100452931 |
| authorships[7].author.orcid | https://orcid.org/0000-0002-6460-8563 |
| authorships[7].author.display_name | Prashant Kumar |
| authorships[7].author_position | middle |
| authorships[7].raw_author_name | Kumar, Sathish |
| authorships[7].is_corresponding | False |
| authorships[8].author.id | https://openalex.org/A5068771985 |
| authorships[8].author.orcid | https://orcid.org/0000-0002-5964-2329 |
| authorships[8].author.display_name | Rina Barouch‐Bentov |
| authorships[8].author_position | middle |
| authorships[8].raw_author_name | Barouch-Bentov, Rina |
| authorships[8].is_corresponding | False |
| authorships[9].author.id | https://openalex.org/A5052214218 |
| authorships[9].author.orcid | https://orcid.org/0000-0002-7685-6302 |
| authorships[9].author.display_name | Olga González‐López |
| authorships[9].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[9].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[9].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[9].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[9].institutions[0].type | healthcare |
| authorships[9].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[9].institutions[0].country_code | |
| authorships[9].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[9].author_position | middle |
| authorships[9].raw_author_name | González-López, Olga |
| authorships[9].is_corresponding | False |
| authorships[9].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[10].author.id | https://openalex.org/A5074894886 |
| authorships[10].author.orcid | https://orcid.org/0000-0002-8866-3532 |
| authorships[10].author.display_name | Ryan P. McNamara |
| authorships[10].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[10].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[10].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[10].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[10].institutions[0].type | healthcare |
| authorships[10].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[10].institutions[0].country_code | |
| authorships[10].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[10].author_position | middle |
| authorships[10].raw_author_name | McNamara, Ryan |
| authorships[10].is_corresponding | False |
| authorships[10].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[11].author.id | https://openalex.org/A5100336169 |
| authorships[11].author.orcid | https://orcid.org/0000-0003-0899-5703 |
| authorships[11].author.display_name | Li Wang |
| authorships[11].affiliations[0].raw_affiliation_string | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[11].author_position | middle |
| authorships[11].raw_author_name | Wang, Li |
| authorships[11].is_corresponding | False |
| authorships[11].raw_affiliation_strings | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[12].author.id | https://openalex.org/A5025397159 |
| authorships[12].author.orcid | https://orcid.org/0000-0002-2593-6003 |
| authorships[12].author.display_name | Adriana Hertel-Wulff |
| authorships[12].affiliations[0].institution_ids | https://openalex.org/I4390039329 |
| authorships[12].affiliations[0].raw_affiliation_string | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[12].institutions[0].id | https://openalex.org/I4390039329 |
| authorships[12].institutions[0].ror | https://ror.org/043ehm030 |
| authorships[12].institutions[0].type | healthcare |
| authorships[12].institutions[0].lineage | https://openalex.org/I114027177, https://openalex.org/I4390039329 |
| authorships[12].institutions[0].country_code | |
| authorships[12].institutions[0].display_name | UNC Lineberger Comprehensive Cancer Center |
| authorships[12].author_position | middle |
| authorships[12].raw_author_name | Hertel-Wulff, Adriana |
| authorships[12].is_corresponding | False |
| authorships[12].raw_affiliation_strings | N.C. Cancer Hospital, UNC Lineberger Comprehensive Cancer Center |
| authorships[13].author.id | https://openalex.org/A5100422524 |
| authorships[13].author.orcid | https://orcid.org/0000-0002-0731-8930 |
| authorships[13].author.display_name | Xian Chen |
| authorships[13].affiliations[0].raw_affiliation_string | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[13].author_position | middle |
| authorships[13].raw_author_name | Chen, Xian |
| authorships[13].is_corresponding | False |
| authorships[13].raw_affiliation_strings | School of Medicine, Department of Biochemistry and Biophysics |
| authorships[14].author.id | https://openalex.org/A5031150507 |
| authorships[14].author.orcid | https://orcid.org/0000-0001-6441-4171 |
| authorships[14].author.display_name | Shirit Einav |
| authorships[14].author_position | middle |
| authorships[14].raw_author_name | Einav, Shirit |
| authorships[14].is_corresponding | False |
| authorships[15].author.id | https://openalex.org/A5028921086 |
| authorships[15].author.orcid | https://orcid.org/0000-0002-4438-2018 |
| authorships[15].author.display_name | Joseph A. Duncan |
| authorships[15].affiliations[0].raw_affiliation_string | School of Medicine, Department of Medicine |
| authorships[15].author_position | middle |
| authorships[15].raw_author_name | Duncan, Joseph A. |
| authorships[15].is_corresponding | False |
| authorships[15].raw_affiliation_strings | School of Medicine, Department of Medicine |
| authorships[16].author.id | https://openalex.org/A5020375717 |
| authorships[16].author.orcid | https://orcid.org/0000-0002-6906-4163 |
| authorships[16].author.display_name | Maryna Kapustina |
| authorships[16].affiliations[0].raw_affiliation_string | School of Medicine, Department of Cell Biology and Physiology |
| authorships[16].author_position | middle |
| authorships[16].raw_author_name | Kapustina, Maryna |
| authorships[16].is_corresponding | False |
| authorships[16].raw_affiliation_strings | School of Medicine, Department of Cell Biology and Physiology |
| authorships[17].author.id | https://openalex.org/A5078717593 |
| authorships[17].author.orcid | https://orcid.org/0000-0001-9754-5303 |
| authorships[17].author.display_name | Elizabeth E. Fry |
| authorships[17].author_position | middle |
| authorships[17].raw_author_name | Fry, Elizabeth E. |
| authorships[17].is_corresponding | False |
| authorships[18].author.id | https://openalex.org/A5056016799 |
| authorships[18].author.orcid | https://orcid.org/0000-0002-3426-4210 |
| authorships[18].author.display_name | David I. Stuart |
| authorships[18].author_position | middle |
| authorships[18].raw_author_name | Stuart, David I. |
| authorships[18].is_corresponding | False |
| authorships[19].author.id | https://openalex.org/A5026233059 |
| authorships[19].author.orcid | https://orcid.org/0000-0003-1450-806X |
| authorships[19].author.display_name | Stanley M. Lemon |
| authorships[19].affiliations[0].raw_affiliation_string | School of Medicine, Department of Medicine |
| authorships[19].author_position | last |
| authorships[19].raw_author_name | Lemon, Stanley M. |
| authorships[19].is_corresponding | False |
| authorships[19].raw_affiliation_strings | School of Medicine, Department of Medicine |
| has_content.pdf | False |
| has_content.grobid_xml | False |
| is_paratext | False |
| open_access.is_oa | True |
| open_access.oa_url | https://doi.org/10.17615/cc9h-0b78 |
| open_access.oa_status | green |
| open_access.any_repository_has_fulltext | False |
| created_date | 2025-10-10T00:00:00 |
| display_name | Nonlytic cellular release of hepatitis A virus requires dual capsid recruitment of the ESCRT-associated Bro1 domain proteins HD-PTP and ALIX |
| has_fulltext | True |
| is_retracted | False |
| updated_date | 2025-11-06T06:51:31.235846 |
| primary_topic.id | https://openalex.org/T12025 |
| primary_topic.field.id | https://openalex.org/fields/27 |
| primary_topic.field.display_name | Medicine |
| primary_topic.score | 0.9994000196456909 |
| primary_topic.domain.id | https://openalex.org/domains/4 |
| primary_topic.domain.display_name | Health Sciences |
| primary_topic.subfield.id | https://openalex.org/subfields/2721 |
| primary_topic.subfield.display_name | Hepatology |
| primary_topic.display_name | Hepatitis Viruses Studies and Epidemiology |
| related_works | https://openalex.org/W1973572007, https://openalex.org/W2971717878, https://openalex.org/W91867460, https://openalex.org/W2109627615, https://openalex.org/W2074582729, https://openalex.org/W1965355812, https://openalex.org/W2144314464, https://openalex.org/W2026933690, https://openalex.org/W2925209159, https://openalex.org/W2010767491 |
| cited_by_count | 0 |
| locations_count | 1 |
| best_oa_location.id | doi:10.17615/cc9h-0b78 |
| best_oa_location.is_oa | True |
| best_oa_location.source.id | https://openalex.org/S7407051488 |
| best_oa_location.source.type | repository |
| best_oa_location.source.is_oa | False |
| best_oa_location.source.issn_l | |
| best_oa_location.source.is_core | False |
| best_oa_location.source.is_in_doaj | False |
| best_oa_location.source.display_name | UNC Libraries |
| best_oa_location.source.host_organization | |
| best_oa_location.source.host_organization_name | |
| best_oa_location.license | |
| best_oa_location.pdf_url | |
| best_oa_location.version | |
| best_oa_location.raw_type | article-journal |
| best_oa_location.license_id | |
| best_oa_location.is_accepted | False |
| best_oa_location.is_published | False |
| best_oa_location.raw_source_name | |
| best_oa_location.landing_page_url | https://doi.org/10.17615/cc9h-0b78 |
| primary_location.id | doi:10.17615/cc9h-0b78 |
| primary_location.is_oa | True |
| primary_location.source.id | https://openalex.org/S7407051488 |
| primary_location.source.type | repository |
| primary_location.source.is_oa | False |
| primary_location.source.issn_l | |
| primary_location.source.is_core | False |
| primary_location.source.is_in_doaj | False |
| primary_location.source.display_name | UNC Libraries |
| primary_location.source.host_organization | |
| primary_location.source.host_organization_name | |
| primary_location.license | |
| primary_location.pdf_url | |
| primary_location.version | |
| primary_location.raw_type | article-journal |
| primary_location.license_id | |
| primary_location.is_accepted | False |
| primary_location.is_published | False |
| primary_location.raw_source_name | |
| primary_location.landing_page_url | https://doi.org/10.17615/cc9h-0b78 |
| publication_date | 2022-09-03 |
| publication_year | 2022 |
| referenced_works_count | 0 |
| abstract_inverted_index.8 | 75 |
| abstract_inverted_index.A | 35 |
| abstract_inverted_index.X | 200 |
| abstract_inverted_index.a | 68, 84, 97, 114, 136, 160, 211 |
| abstract_inverted_index.23 | 209 |
| abstract_inverted_index.24 | 115 |
| abstract_inverted_index.We | 57 |
| abstract_inverted_index.an | 52, 276 |
| abstract_inverted_index.as | 185 |
| abstract_inverted_index.in | 17, 55, 64, 83, 104, 108, 146, 156, 168 |
| abstract_inverted_index.is | 154 |
| abstract_inverted_index.of | 7, 32, 41, 60, 90, 124, 163, 219, 227, 240, 268, 285, 295 |
| abstract_inverted_index.pX | 79, 95, 125, 151, 169, 257 |
| abstract_inverted_index.to | 87, 96, 176, 217 |
| abstract_inverted_index.we | 29 |
| abstract_inverted_index.Our | 273 |
| abstract_inverted_index.The | 20, 150 |
| abstract_inverted_index.VP1 | 78 |
| abstract_inverted_index.and | 130, 166, 202, 246, 253, 271, 289, 298 |
| abstract_inverted_index.are | 2, 11, 25, 183 |
| abstract_inverted_index.bat | 172 |
| abstract_inverted_index.for | 47, 132 |
| abstract_inverted_index.its | 105, 203 |
| abstract_inverted_index.kDa | 76 |
| abstract_inverted_index.the | 33, 74, 122, 177, 261 |
| abstract_inverted_index.was | 127 |
| abstract_inverted_index.ALIX | 245 |
| abstract_inverted_index.Bro1 | 213, 229, 266 |
| abstract_inverted_index.YxxL | 137 |
| abstract_inverted_index.acid | 117 |
| abstract_inverted_index.both | 128, 269, 296 |
| abstract_inverted_index.eHAV | 143, 233 |
| abstract_inverted_index.from | 14, 159, 171 |
| abstract_inverted_index.host | 42 |
| abstract_inverted_index.into | 222 |
| abstract_inverted_index.late | 88 |
| abstract_inverted_index.play | 51 |
| abstract_inverted_index.role | 54 |
| abstract_inverted_index.show | 58 |
| abstract_inverted_index.that | 50, 81, 126 |
| abstract_inverted_index.this | 23, 140 |
| abstract_inverted_index.type | 208 |
| abstract_inverted_index.when | 174 |
| abstract_inverted_index.wide | 161 |
| abstract_inverted_index.with | 39, 195, 243, 264 |
| abstract_inverted_index.(HAV) | 37 |
| abstract_inverted_index.ALIX. | 272, 299 |
| abstract_inverted_index.Here, | 28 |
| abstract_inverted_index.amino | 116 |
| abstract_inverted_index.cargo | 221 |
| abstract_inverted_index.cells | 16 |
| abstract_inverted_index.fused | 175 |
| abstract_inverted_index.motif | 138 |
| abstract_inverted_index.range | 162 |
| abstract_inverted_index.shows | 290 |
| abstract_inverted_index.study | 274 |
| abstract_inverted_index.these | 181 |
| abstract_inverted_index.using | 250 |
| abstract_inverted_index.viral | 241, 279 |
| abstract_inverted_index.virus | 36, 62, 147 |
| abstract_inverted_index.(eHAV) | 63 |
| abstract_inverted_index.Fusing | 94 |
| abstract_inverted_index.HD-PTP | 270, 297 |
| abstract_inverted_index.assays | 249 |
| abstract_inverted_index.capsid | 38 |
| abstract_inverted_index.center | 123 |
| abstract_inverted_index.domain | 214, 230 |
| abstract_inverted_index.either | 228 |
| abstract_inverted_index.export | 70, 152, 262, 280 |
| abstract_inverted_index.genera | 10 |
| abstract_inverted_index.linked | 216 |
| abstract_inverted_index.manner | 85 |
| abstract_inverted_index.poorly | 26 |
| abstract_inverted_index.potent | 278 |
| abstract_inverted_index.second | 212 |
| abstract_inverted_index.signal | 71, 153, 263, 281 |
| abstract_inverted_index.within | 73, 121, 139 |
| abstract_inverted_index.(ALIX), | 201 |
| abstract_inverted_index.(ESCRT) | 49 |
| abstract_inverted_index.EPN-pX, | 196 |
| abstract_inverted_index.HD-PTP. | 247 |
| abstract_inverted_index.ablated | 142 |
| abstract_inverted_index.capsids | 242 |
| abstract_inverted_index.domains | 89, 267 |
| abstract_inverted_index.impeded | 232 |
| abstract_inverted_index.located | 72, 120 |
| abstract_inverted_index.members | 6 |
| abstract_inverted_index.peptide | 118 |
| abstract_inverted_index.process | 24 |
| abstract_inverted_index.protein | 100, 199, 215, 231, 287 |
| abstract_inverted_index.release | 59, 107, 284, 291 |
| abstract_inverted_index.sorting | 44, 218 |
| abstract_inverted_index.through | 260 |
| abstract_inverted_index.viruses | 182 |
| abstract_inverted_index.(EPN-pX) | 102 |
| abstract_inverted_index.Although | 0 |
| abstract_inverted_index.Deleting | 135 |
| abstract_inverted_index.analysis | 112 |
| abstract_inverted_index.describe | 30 |
| abstract_inverted_index.directly | 259 |
| abstract_inverted_index.infected | 15 |
| abstract_inverted_index.multiple | 8, 191 |
| abstract_inverted_index.nanocage | 101, 133, 178 |
| abstract_inverted_index.paralog, | 204 |
| abstract_inverted_index.peptides | 252 |
| abstract_inverted_index.protein, | 179 |
| abstract_inverted_index.proteins | 193, 255 |
| abstract_inverted_index.release, | 144 |
| abstract_inverted_index.release. | 56, 134, 234 |
| abstract_inverted_index.released | 12, 184 |
| abstract_inverted_index.required | 46 |
| abstract_inverted_index.requires | 67, 292 |
| abstract_inverted_index.resulted | 103 |
| abstract_inverted_index.revealed | 256 |
| abstract_inverted_index.sequence | 119, 141 |
| abstract_inverted_index.species, | 165 |
| abstract_inverted_index.vesicles | 66 |
| abstract_inverted_index.virions. | 187 |
| abstract_inverted_index.viruses. | 93 |
| abstract_inverted_index.(HD-PTP), | 210 |
| abstract_inverted_index.analogous | 86 |
| abstract_inverted_index.canonical | 91 |
| abstract_inverted_index.complexes | 45 |
| abstract_inverted_index.conserved | 69, 155 |
| abstract_inverted_index.depletion | 226 |
| abstract_inverted_index.endosomal | 43 |
| abstract_inverted_index.enveloped | 92 |
| abstract_inverted_index.essential | 53 |
| abstract_inverted_index.extension | 80 |
| abstract_inverted_index.functions | 82 |
| abstract_inverted_index.hepatitis | 34 |
| abstract_inverted_index.including | 197 |
| abstract_inverted_index.interacts | 258 |
| abstract_inverted_index.mammalian | 164 |
| abstract_inverted_index.mediating | 282 |
| abstract_inverted_index.necessary | 129 |
| abstract_inverted_index.non-human | 157 |
| abstract_inverted_index.resulting | 145 |
| abstract_inverted_index.sequences | 170 |
| abstract_inverted_index.transport | 48 |
| abstract_inverted_index.vesicles. | 19, 110 |
| abstract_inverted_index.C-terminal | 77 |
| abstract_inverted_index.Mutational | 111 |
| abstract_inverted_index.N-terminal | 265 |
| abstract_inverted_index.activities | 294 |
| abstract_inverted_index.assemblies | 288 |
| abstract_inverted_index.components | 40 |
| abstract_inverted_index.considered | 4 |
| abstract_inverted_index.endogenous | 244 |
| abstract_inverted_index.endosomes. | 224 |
| abstract_inverted_index.engineered | 99 |
| abstract_inverted_index.functional | 167 |
| abstract_inverted_index.identified | 113, 190 |
| abstract_inverted_index.identifies | 275 |
| abstract_inverted_index.mechanisms | 21 |
| abstract_inverted_index.microscopy | 237 |
| abstract_inverted_index.proteomics | 189 |
| abstract_inverted_index.sufficient | 131 |
| abstract_inverted_index.suggesting | 180 |
| abstract_inverted_index.underlying | 22 |
| abstract_inverted_index.associating | 194 |
| abstract_inverted_index.phosphatase | 206 |
| abstract_inverted_index.recombinant | 254 |
| abstract_inverted_index.understood. | 27 |
| abstract_inverted_index.virus-sized | 286 |
| abstract_inverted_index.Quantitative | 188 |
| abstract_inverted_index.accumulating | 148 |
| abstract_inverted_index.demonstrated | 238 |
| abstract_inverted_index.exosome-like | 65 |
| abstract_inverted_index.fluorescence | 236 |
| abstract_inverted_index.interactions | 31 |
| abstract_inverted_index.non-receptor | 207 |
| abstract_inverted_index.nonlytically | 13 |
| abstract_inverted_index.picornaviral | 9 |
| abstract_inverted_index.ESCRT-related | 192 |
| abstract_inverted_index.RNAi-mediated | 225 |
| abstract_inverted_index.biotin-tagged | 251 |
| abstract_inverted_index.exceptionally | 277 |
| abstract_inverted_index.extracellular | 18, 109, 283 |
| abstract_inverted_index.hepatoviruses | 158, 173 |
| abstract_inverted_index.non-redundant | 293 |
| abstract_inverted_index.ubiquitylated | 220 |
| abstract_inverted_index.colocalization | 239 |
| abstract_inverted_index.conventionally | 3 |
| abstract_inverted_index.multivesicular | 223 |
| abstract_inverted_index.picornaviruses | 1 |
| abstract_inverted_index.ESCRT-dependent | 106 |
| abstract_inverted_index.quasi-enveloped | 61, 186 |
| abstract_inverted_index.self-assembling | 98 |
| abstract_inverted_index.ALG2-interacting | 198 |
| abstract_inverted_index.Super-resolution | 235 |
| abstract_inverted_index.intracellularly. | 149 |
| abstract_inverted_index.tyrosine-protein | 205 |
| abstract_inverted_index.‘nonenveloped’, | 5 |
| abstract_inverted_index.Co-immunoprecipitation | 248 |
| cited_by_percentile_year | |
| countries_distinct_count | 0 |
| institutions_distinct_count | 20 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/3 |
| sustainable_development_goals[0].score | 0.44999998807907104 |
| sustainable_development_goals[0].display_name | Good health and well-being |
| citation_normalized_percentile.value | 0.18039188 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | False |