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Article: High transmission of endemic human coronaviruses before and during the COVID-19 pandemic in adolescents in Cebu, Philippines.

Joseph, Janet O / Ylade, Michelle / Daag, Jedas Veronica / Aogo, Rosemary / Crisostomo, Maria Vinna / Mpingabo, Patrick / Premkumar, Lakshmanane / Deen, Jacqueline / Katzelnick, Leah

Research square

2023

Abstract: Background: SARS-CoV-2, the causative agent of COVID-19, is a betacoronavirus belonging to the same genus as endemic human coronaviruses (hCoVs) OC43 and HKU1 and is distinct from alpha hCoVs 229E and NL63. In a study of adolescents in the Philippines, ... ...

Abstract	Background: SARS-CoV-2, the causative agent of COVID-19, is a betacoronavirus belonging to the same genus as endemic human coronaviruses (hCoVs) OC43 and HKU1 and is distinct from alpha hCoVs 229E and NL63. In a study of adolescents in the Philippines, we evaluated the seroprevalence to hCoVs, whether pre-pandemic hCoV immunity modulated subsequent risk of SARS-CoV-2 infection, and if SARS-CoV-2 infection affected the transmission of the hCoVs. Methods: From 499 samples collected in 2021 and screened by SARS-CoV-2 receptor binding domain (RBD) enzyme-linked immunosorbent assay (ELISA), we randomly selected 59 SARS-CoV-2 negative and 61 positive individuals for further serological evaluation. We measured RBD and spike antibodies to the four hCoVs and SARS-CoV-2 by ELISA in samples from the same participants collected pre-pandemic (2018-2019) and mid-pandemic (2021), before COVID-19 vaccination. Results: We observed over 72% seropositivity to the four hCoVs pre-pandemic. Binding antibodies increased with age to 229E and OC43, suggesting endemic circulation, while immunity was flat across ages for HKU1 and NL63. During the COVID-19 pandemic, antibody level increased significantly to the RBDs of OC43, NL63, and 229E and spikes of all four hCoVs in both SARS-CoV-2 negative and positive adolescents. Those aged 12-15 years old in 2021 had higher antibodies to RBD and spike of OC43, NL63, and 229E than adolescents the same age in 2019, further demonstrating intense transmission of the hCoVs during the pandemic. Conclusions: We observe a limited impact of the COVID-19 pandemic on endemic hCoV transmission. This study provides insight into co-circulation of hCoVs and SARS-CoV-2.
Language	English
Publishing date	2023-11-16
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-3581033/v1
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Article ; Online: SARS-CoV-2 Seroprevalence: Demographic and Behavioral Factors Associated With Seropositivity Among College Students in a University Setting.

Diepstra, Karen / Bullington, Brooke W / Premkumar, Lakshmanane / Shook-Sa, Bonnie E / Jones, Corbin / Pettifor, Audrey

The Journal of adolescent health : official publication of the Society for Adolescent Medicine

2022 Volume 71, Issue 5, Page(s) 559–569

Abstract: Purpose: Examine SARS-CoV-2 seroprevalence and the association of seropositivity with demographic, geographic, and behavioral variables among University of North Carolina Chapel Hill (UNC-CH) undergraduate students enrolled in the fall 2020 semester.: ...

Abstract	Purpose: Examine SARS-CoV-2 seroprevalence and the association of seropositivity with demographic, geographic, and behavioral variables among University of North Carolina Chapel Hill (UNC-CH) undergraduate students enrolled in the fall 2020 semester. Methods: All UNC-CH undergraduate students were invited to participate in the Heelcheck study; participants were weighted to the UNC-CH undergraduate population using raking methods. We estimate SARS-CoV-2 seroprevalence at study entrance (11/12/2020-12/10/2020) and bivariable associations using log-binomial regression. Results: SARS-CoV-2 seroprevalence was 7.3% (95% confidence interval (CI): 5.4%-9.2%) at baseline. Compared to students who were living off-campus in the Chapel Hill/Carrboro area (CH) for the Fall 2020 semester (8.6% seroprevalence), students who never returned to CH had lower seroprevalence (1.9%, prevalence ratio (PR), 95% CI: 0.22, 0.06-0.81), whereas, students who started the semester on-campus and moved to off-campus CH housing had 18.9% seroprevalence (PR, 95% CI: 2.21, 1.04-4.72) and students who spent the semester living in a Sorority/Fraternity house had 46.8% seroprevalence (PR, 95% CI: 5.47, 2.62-11.46). Those who predicted they would join an indoor party unmasked had 3.8 times the seroprevalence of those who indicated they would not attend (PR, 95% CI: 3.80, 1.58-9.16). Compared to students who disagreed with the statement "…I am not going to let COVID-19 stop me from having fun…", those who agreed had higher seroprevalence (14.0% vs. 5.7%; (PR, 95% CI: 2.45, 1.13-5.32)). Discussion: Increased seroprevalence was associated with congregate living and participation (actual or endorsed) in social activities. During pandemics, universities must create safe socializing opportunities while minimizing transmission.
MeSH term(s)	Humans ; SARS-CoV-2 ; Universities ; Seroepidemiologic Studies ; COVID-19 ; Students ; Demography
Language	English
Publishing date	2022-07-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1063374-1
ISSN	1879-1972 ; 1054-139X
ISSN (online)	1879-1972
ISSN	1054-139X
DOI	10.1016/j.jadohealth.2022.06.015
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Article: Inapparent primary dengue virus infections reveal hidden serotype-specific epidemiological patterns and spectrum of infection outcome: a cohort study in Nicaragua.

Bos, Sandra / Zambrana, Jose Victor / Duarte, Elias / Graber, Aaron L / Huffaker, Julia / Montenegro, Carlos / Premkumar, Lakshmanane / Gordon, Aubree / Balmaseda, Angel / Harris, Eva

medRxiv : the preprint server for health sciences

2024

Abstract: Background: Dengue is the most prevalent mosquito-borne viral disease and a major public health problem worldwide. Most primary infections with the four dengue virus serotypes (DENV1-4) are inapparent; nevertheless, prior research has primarily focused ... ...

Abstract	Background: Dengue is the most prevalent mosquito-borne viral disease and a major public health problem worldwide. Most primary infections with the four dengue virus serotypes (DENV1-4) are inapparent; nevertheless, prior research has primarily focused on symptomatic infections, which has limited our understanding of the epidemiological burden and spectrum of disease of each DENV serotype. Our study addresses this bottleneck in dengue research by providing a new method and a detailed examination of primary inapparent infections. Methods: Here we present (1) the evaluation of a multiplex DENV1-4 envelope domain III multiplex microsphere-based assay (EDIII-MMBA) to serotype inapparent primary infections and (2) its application leveraging 17 years of prospective sample collection from the Nicaraguan Pediatric Dengue Cohort Study. After evaluation, we analyzed 46% (N=574) of total inapparent primary DENV infections with the EDIII-MMBA. Remaining infections were inferred using stochastic imputation, taking year and neighborhood of infection into account. Findings: The EDIII-MMBA demonstrated excellent diagnostic accuracy of symptomatic and inapparent primary DENV infections when evaluated against gold-standard serotyping methods. Significant within- and between-year variation in serotype distribution between symptomatic and inapparent infections and circulation of serotypes undetected in symptomatic cases were observed in multiple years. Our findings reveal that a significant majority of primary infections remained inapparent: 76.8% for DENV1, 79.9% for DENV2, and 63.9% for DENV3. DENV3 exhibited the highest likelihood of symptomatic and severe primary infections (Pooled OR compared to DENV1 = 2.13, 95% CI 1.28-3.56, and 6.75, 2.01-22.62, respectively), whereas DENV2 had similar likelihood to DENV1 in both analyses. Interpretation: Our study indicates that case surveillance skews the perceived epidemiological footprint of DENV and reveals a more complex and intricate pattern of serotype distribution in inapparent infections. Further, the significant differences in infection outcomes by serotype emphasizes the need for serotype-informed public health strategies. Funding: NIH/NIAID P01AI106695, U01AI153416. Research in context: Evidence before this study:
Language	English
Publishing date	2024-04-08
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.04.05.24305281
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Article ; Online: Antibody Immunity to Zika Virus among Young Children in a Flavivirus-Endemic Area in Nicaragua.

Zepeda, Omar / Espinoza, Daniel O / Martinez, Evelin / Cross, Kaitlyn A / Becker-Dreps, Sylvia / de Silva, Aravinda M / Bowman, Natalie M / Premkumar, Lakshmanane / Stringer, Elizabeth M / Bucardo, Filemón / Collins, Matthew H

Viruses

2023 Volume 15, Issue 3

Abstract: Objective: ...

Abstract	Objective:
MeSH term(s)	Infant ; Infant, Newborn ; Female ; Humans ; Child ; Pregnancy ; Child, Preschool ; Zika Virus ; Flavivirus ; Zika Virus Infection ; Nicaragua/epidemiology ; Dengue Virus ; Antibodies, Viral ; Immunoglobulin G ; Cross Reactions ; Dengue
Chemical Substances	Antibodies, Viral ; Immunoglobulin G
Language	English
Publishing date	2023-03-21
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v15030796
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Article: Targets and cross-reactivity of human T cell recognition of Common Cold Coronaviruses.

Tarke, Alison / Zhang, Yun / Methot, Nils / Narowski, Tara M / Phillips, Elizabeth / Mallal, Simon / Frazier, April / Filaci, Gilberto / Weiskopf, Daniela / Dan, Jennifer M / Premkumar, Lakshmanane / Scheuermann, Richard H / Sette, Alessandro / Grifoni, Alba

bioRxiv : the preprint server for biology

2023

Abstract: The Coronavirus (CoV) family includes a variety of viruses able to infect humans. Endemic CoVs that can cause common cold belong to the alphaCoV and betaCoV genera, with the betaCoV genus also containing subgenera with zoonotic and pandemic concern, ... ...

Abstract	The Coronavirus (CoV) family includes a variety of viruses able to infect humans. Endemic CoVs that can cause common cold belong to the alphaCoV and betaCoV genera, with the betaCoV genus also containing subgenera with zoonotic and pandemic concern, including sarbecoCoV (SARS-CoV and SARS-CoV-2) and merbecoCoV (MERS-CoV). It is therefore warranted to explore pan-CoV vaccine concepts, to provide adaptive immune protection against new potential CoV outbreaks, particularly in the context of betaCoV sub lineages. To explore the feasibility of eliciting CD4
Language	English
Publishing date	2023-01-05
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.04.522794
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Article ; Online: Production of the Receptor-binding Domain of the Viral Spike Proteins from 2003 and 2019 SARS CoVs and the Four Common Human Coronaviruses for Serologic Assays and Inhibitor Screening.

Segovia-Chumbez, Bruno / Graham, Stephen D / Jadi, Ramesh / de Silva, Aravinda M / Premkumar, Lakshmanane

Bio-protocol

2021 Volume 11, Issue 10, Page(s) e4026

Abstract: The recombinant receptor-binding domain (RBD) of the viral spike protein from SARS-CoV-1 and 2 are reliable antigens for detecting viral-specific antibodies in humans. We and others have shown that the levels of RBD-binding antibodies and SARS-CoV-2 ... ...

Abstract	The recombinant receptor-binding domain (RBD) of the viral spike protein from SARS-CoV-1 and 2 are reliable antigens for detecting viral-specific antibodies in humans. We and others have shown that the levels of RBD-binding antibodies and SARS-CoV-2 neutralizing antibodies in patients are correlated. Here, we report the expression and purification of properly folded RBD proteins from SARS and common-cold HCoVs in mammalian cells. RBD proteins were produced with cleavable tags for affinity purification from the cell culture medium and to support multiple immunoassay platforms and drug discovery efforts. Graphic abstract: High-Yield Production of Viral Spike RBDs for Diagnostics and Drug Discovery.
Language	English
Publishing date	2021-05-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	2833269-6
ISSN	2331-8325 ; 2331-8325
ISSN (online)	2331-8325
ISSN	2331-8325
DOI	10.21769/BioProtoc.4026
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Article ; Online: Targets and cross-reactivity of human T cell recognition of common cold coronaviruses.

Cell reports. Medicine

2023 Volume 4, Issue 6, Page(s) 101088

Abstract: The coronavirus (CoV) family includes several viruses infecting humans, highlighting the importance of exploring pan-CoV vaccine strategies to provide broad adaptive immune protection. We analyze T cell reactivity against representative Alpha (NL63) and ... ...

Abstract	The coronavirus (CoV) family includes several viruses infecting humans, highlighting the importance of exploring pan-CoV vaccine strategies to provide broad adaptive immune protection. We analyze T cell reactivity against representative Alpha (NL63) and Beta (OC43) common cold CoVs (CCCs) in pre-pandemic samples. S, N, M, and nsp3 antigens are immunodominant, as shown for severe acute respiratory syndrome 2 (SARS2), while nsp2 and nsp12 are Alpha or Beta specific. We further identify 78 OC43- and 87 NL63-specific epitopes, and, for a subset of those, we assess the T cell capability to cross-recognize sequences from representative viruses belonging to AlphaCoV, sarbecoCoV, and Beta-non-sarbecoCoV groups. We find T cell cross-reactivity within the Alpha and Beta groups, in 89% of the instances associated with sequence conservation >67%. However, despite conservation, limited cross-reactivity is observed for sarbecoCoV, indicating that previous CoV exposure is a contributing factor in determining cross-reactivity. Overall, these results provide critical insights in developing future pan-CoV vaccines.
MeSH term(s)	Humans ; Common Cold ; T-Lymphocytes ; COVID-19 ; SARS-CoV-2 ; Cross Reactions
Language	English
Publishing date	2023-05-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2666-3791
ISSN (online)	2666-3791
DOI	10.1016/j.xcrm.2023.101088
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Article: Magnitude and Durability of the Antibody Response to mRNA-Based Vaccination Among SARS-CoV-2 Seronegative and Seropositive Health Care Personnel.

Open forum infectious diseases

2024 Volume 11, Issue 1, Page(s) ofae009

Abstract: Few studies have described changes in SARS-CoV-2 antibody levels in response to infection and vaccination at frequent intervals and over extended follow-up periods. The purpose of this study was to assess changes in SARS-CoV-2-specific antibody responses ...

Abstract	Few studies have described changes in SARS-CoV-2 antibody levels in response to infection and vaccination at frequent intervals and over extended follow-up periods. The purpose of this study was to assess changes in SARS-CoV-2-specific antibody responses among a prospective cohort of health care personnel over 18 months with up to 22 samples per person. Antibody levels and live virus neutralization were measured before and after mRNA-based vaccination with results stratified by (1) SARS-CoV-2 infection status prior to initial vaccination and (2) SARS-CoV-2 infection at any point during follow-up. We found that the antibody response to the first dose was almost 2-fold higher in individuals who were seropositive prior to vaccination, although neutralization titers were more variable. The antibody response induced by vaccination appeared to wane over time but generally persisted for 8 to 9 months, and those who were infected at any point during the study had slightly higher antibody levels over time vs those who remained uninfected. These findings underscore the need to account for SARS-CoV-2 natural infection as a modifier of vaccine responses, and they highlight the importance of frequent testing of longitudinal antibody titers over time. Together, our results provide a clearer understanding of the trajectories of antibody response among vaccinated individuals with and without prior SARS-CoV-2 infection.
Language	English
Publishing date	2024-01-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2757767-3
ISSN	2328-8957
ISSN	2328-8957
DOI	10.1093/ofid/ofae009
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Article ; Online: Structure and neutralization mechanism of a human antibody targeting a complex Epitope on Zika virus.

Adams, Cameron / Carbaugh, Derek L / Shu, Bo / Ng, Thiam-Seng / Castillo, Izabella N / Bhowmik, Ryan / Segovia-Chumbez, Bruno / Puhl, Ana C / Graham, Stephen / Diehl, Sean A / Lazear, Helen M / Lok, Shee-Mei / de Silva, Aravinda M / Premkumar, Lakshmanane

PLoS pathogens

2023 Volume 19, Issue 1, Page(s) e1010814

Abstract: We currently have an incomplete understanding of why only a fraction of human antibodies that bind to flaviviruses block infection of cells. Here we define the footprint of a strongly neutralizing human monoclonal antibody (mAb G9E) with Zika virus (ZIKV) ...

Abstract	We currently have an incomplete understanding of why only a fraction of human antibodies that bind to flaviviruses block infection of cells. Here we define the footprint of a strongly neutralizing human monoclonal antibody (mAb G9E) with Zika virus (ZIKV) by both X-ray crystallography and cryo-electron microscopy. Flavivirus envelope (E) glycoproteins are present as homodimers on the virion surface, and G9E bound to a quaternary structure epitope spanning both E protomers forming a homodimer. As G9E mainly neutralized ZIKV by blocking a step after viral attachment to cells, we tested if the neutralization mechanism of G9E was dependent on the mAb cross-linking E molecules and blocking low-pH triggered conformational changes required for viral membrane fusion. We introduced targeted mutations to the G9E paratope to create recombinant antibodies that bound to the ZIKV envelope without cross-linking E protomers. The G9E paratope mutants that bound to a restricted epitope on one protomer poorly neutralized ZIKV compared to the wild-type mAb, demonstrating that the neutralization mechanism depended on the ability of G9E to cross-link E proteins. In cell-free low pH triggered viral fusion assay, both wild-type G9E, and epitope restricted paratope mutant G9E bound to ZIKV but only the wild-type G9E blocked fusion. We propose that, beyond antibody binding strength, the ability of human antibodies to cross-link E-proteins is a critical determinant of flavivirus neutralization potency.
MeSH term(s)	Humans ; Zika Virus/genetics ; Epitopes ; Zika Virus Infection ; Antibodies, Neutralizing ; Antibodies, Viral ; Protein Subunits ; Cryoelectron Microscopy ; Viral Envelope Proteins/genetics ; Antibodies, Monoclonal
Chemical Substances	Epitopes ; Antibodies, Neutralizing ; Antibodies, Viral ; Protein Subunits ; Viral Envelope Proteins ; Antibodies, Monoclonal
Language	English
Publishing date	2023-01-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1010814
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Article ; Online: Investigation of the Host Kinome Response to Coronavirus Infection Reveals PI3K/mTOR Inhibitors as Betacoronavirus Antivirals.

Fritch, Ethan J / Mordant, Angie L / Gilbert, Thomas S K / Wells, Carrow I / Yang, Xuan / Barker, Natalie K / Madden, Emily A / Dinnon, Kenneth H / Hou, Yixuan J / Tse, Longping V / Castillo, Izabella N / Sims, Amy C / Moorman, Nathaniel J / Lakshmanane, Premkumar / Willson, Timothy M / Herring, Laura E / Graves, Lee M / Baric, Ralph S

Journal of proteome research

2023 Volume 22, Issue 10, Page(s) 3159–3177

Abstract: Host kinases play essential roles in the host cell cycle, innate immune signaling, the stress response to viral infection, and inflammation. Previous work has demonstrated that coronaviruses specifically target kinase cascades to subvert host cell ... ...

Abstract	Host kinases play essential roles in the host cell cycle, innate immune signaling, the stress response to viral infection, and inflammation. Previous work has demonstrated that coronaviruses specifically target kinase cascades to subvert host cell responses to infection and rely upon host kinase activity to phosphorylate viral proteins to enhance replication. Given the number of kinase inhibitors that are already FDA approved to treat cancers, fibrosis, and other human disease, they represent an attractive class of compounds to repurpose for host-targeted therapies against emerging coronavirus infections. To further understand the host kinome response to betacoronavirus infection, we employed multiplex inhibitory bead mass spectrometry (MIB-MS) following MERS-CoV and SARS-CoV-2 infection of human lung epithelial cell lines. Our MIB-MS analyses revealed activation of mTOR and MAPK signaling following MERS-CoV and SARS-CoV-2 infection, respectively. SARS-CoV-2 host kinome responses were further characterized using paired phosphoproteomics, which identified activation of MAPK, PI3K, and mTOR signaling. Through chemogenomic screening, we found that clinically relevant PI3K/mTOR inhibitors were able to inhibit coronavirus replication at nanomolar concentrations similar to direct-acting antivirals. This study lays the groundwork for identifying broad-acting, host-targeted therapies to reduce betacoronavirus replication that can be rapidly repurposed during future outbreaks and epidemics. The proteomics, phosphoproteomics, and MIB-MS datasets generated in this study are available in the Proteomics Identification Database (PRIDE) repository under project identifiers PXD040897 and PXD040901.
MeSH term(s)	Humans ; Antiviral Agents/pharmacology ; COVID-19 ; MTOR Inhibitors ; Phosphatidylinositol 3-Kinases ; SARS-CoV-2 ; Virus Replication ; Hepatitis C, Chronic ; Middle East Respiratory Syndrome Coronavirus/physiology ; TOR Serine-Threonine Kinases
Chemical Substances	Antiviral Agents ; MTOR Inhibitors ; Phosphatidylinositol 3-Kinases (EC 2.7.1.-) ; TOR Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2023-08-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.3c00182
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