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Article ; Online: The multifaceted roles of breast milk antibodies.

Atyeo, Caroline / Alter, Galit

2021 Volume 184, Issue 6, Page(s) 1486–1499

Abstract: Neonates are born with an immature immune system and rely on the transfer of immunity from their mothers. Maternal antibodies are transferred via the placenta and breast milk. Although the role of placentally transferred immunoglobulin G (IgG) is ... ...

Abstract	Neonates are born with an immature immune system and rely on the transfer of immunity from their mothers. Maternal antibodies are transferred via the placenta and breast milk. Although the role of placentally transferred immunoglobulin G (IgG) is established, less is known about the selection of antibodies transferred via breast milk and the mechanisms by which they provide protection against neonatal disease. Evidence suggests that breast milk antibodies play multifaceted roles, preventing infection and supporting the selection of commensals and tolerizing immunity during infancy. Here, we discuss emerging data related to the importance of breast milk antibodies in neonatal immunity and development.
MeSH term(s)	Animals ; Antibodies/metabolism ; Homeostasis ; Humans ; Immunity ; Immunologic Factors/pharmacology ; Microbiota ; Milk, Human/immunology
Chemical Substances	Antibodies ; Immunologic Factors
Language	English
Publishing date	2021-03-31
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2021.02.031
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Article ; Online: A Single-Dose Intranasal Combination Panebolavirus Vaccine.

Malherbe, Delphine C / Kimble, J Brian / Atyeo, Caroline / Fischinger, Stephanie / Meyer, Michelle / Cody, S Gabrielle / Hyde, Matthew / Alter, Galit / Bukreyev, Alexander

The Journal of infectious diseases

2023 Volume 228, Issue Suppl 7, Page(s) S648–S659

Abstract: Background: Ebolaviruses Ebola (EBOV), Sudan (SUDV), and Bundibugyo (BDBV) cause severe human disease, which may be accompanied by hemorrhagic syndrome, with high case fatality rates. Monovalent vaccines do not offer cross-protection against these ... ...

Abstract	Background: Ebolaviruses Ebola (EBOV), Sudan (SUDV), and Bundibugyo (BDBV) cause severe human disease, which may be accompanied by hemorrhagic syndrome, with high case fatality rates. Monovalent vaccines do not offer cross-protection against these viruses whose endemic areas overlap. Therefore, development of a panebolavirus vaccine is a priority. As a vaccine vector, human parainfluenza virus type 3 (HPIV3) has the advantages of needle-free administration and induction of both systemic and local mucosal antibody responses in the respiratory tract. Methods: To minimize the antivector immunity, genes encoding the HPIV3 envelope proteins F and HN were removed from the vaccine constructs, resulting in expression of only the ebolavirus envelope protein-glycoprotein. These second-generation vaccine constructs were used to develop a combination vaccine against EBOV, SUDV, and BDBV. Results: A single intranasal vaccination of guinea pigs or ferrets with the trivalent combination vaccine elicited humoral responses to each of the targeted ebolaviruses, including binding and neutralizing antibodies, as well as Fc-mediated effector functions. This vaccine protected animals from death and disease caused by lethal challenges with EBOV, SUDV, or BDBV. Conclusions: The combination vaccine elicited protection that was comparable to that induced by the monovalent vaccines, thus demonstrating the value of this combination trivalent vaccine.
MeSH term(s)	Animals ; Humans ; Guinea Pigs ; Antibodies, Viral ; Ebola Vaccines ; Ferrets ; Hemorrhagic Fever, Ebola ; Ebolavirus ; Antibodies, Neutralizing ; Vaccines, Combined
Chemical Substances	Antibodies, Viral ; Ebola Vaccines ; Antibodies, Neutralizing ; Vaccines, Combined
Language	English
Publishing date	2023-07-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiad266
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Article ; Online: Preserved recognition of Omicron spike following COVID-19 messenger RNA vaccination in pregnancy.

Bartsch, Yannic C / Atyeo, Caroline / Kang, Jaewon / Cai, Yongfei / Chen, Bing / Gray, Kathryn J / Edlow, Andrea G / Alter, Galit

American journal of obstetrics and gynecology

2022 Volume 227, Issue 3, Page(s) 493.e1–493.e7

Abstract: Background: SARS-CoV-2 infection is associated with enhanced disease severity in pregnant women. Despite the potential of COVID-19 vaccines to reduce severe disease, vaccine uptake remained relatively low among pregnant women. Just as coordinated ... ...

Abstract	Background: SARS-CoV-2 infection is associated with enhanced disease severity in pregnant women. Despite the potential of COVID-19 vaccines to reduce severe disease, vaccine uptake remained relatively low among pregnant women. Just as coordinated messaging from the Centers for Disease Control and Prevention and leading obstetrics organizations began to increase vaccine confidence in this vulnerable group, the evolution of SARS-CoV-2 variants of concerns, including the Omicron variant, raised new concerns about vaccine efficacy because of their ability to escape vaccine-induced neutralizing antibodies. Early data point to a milder disease course following infection with the Omicron variant in vaccinated individuals. Thus, these data suggest that alternate vaccine-induced immunity beyond neutralization may continue to attenuate Omicron variant-induced disease, such as Fc-mediated antibody activity. Objective: This study aimed to test whether vaccine-induced antibodies raised during pregnancy continue to bind to and leverage Fc receptors to protect against variants of concern including the Omicron variant. Study design: The receptor binding domain or whole spike-specific antibody isotype binding titers and Fc gamma receptor binding directed toward variants of concern, including the Omicron variant, were analyzed in pregnant women after receiving the full dose regimen of either the Pfizer/BioNTech BNT62b2 (n=10) or Moderna mRNA-1273 (n=10) vaccination using a multiplexing Luminex assay. Results: Reduced isotype recognition of the Omicron receptor binding domain was observed following administration of either vaccine with relatively preserved, albeit reduced, recognition of the whole Omicron spike by immunoglobulin M and G antibodies. Despite the near complete loss of Fc receptor binding to the Omicron receptor binding domain, Fc receptor binding to the Omicron spike was more variable but largely preserved. Conclusion: Reduced binding titers to the Omicron receptor binding domain aligns with the observed loss of neutralizing activity. Despite the loss of neutralization, preserved, albeit reduced, Omicron spike recognition and Fc receptor binding potentially continue to attenuate disease severity in pregnant women.
MeSH term(s)	Antibodies, Viral ; COVID-19/prevention & control ; COVID-19 Vaccines ; Female ; Humans ; Membrane Glycoproteins/genetics ; Membrane Glycoproteins/metabolism ; Pregnancy ; Pregnancy Complications, Infectious/prevention & control ; RNA, Messenger ; Receptors, Fc ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus/genetics ; Vaccination ; Vaccines ; Viral Envelope Proteins/genetics ; Viral Envelope Proteins/metabolism
Chemical Substances	Antibodies, Viral ; COVID-19 Vaccines ; Membrane Glycoproteins ; RNA, Messenger ; Receptors, Fc ; Spike Glycoprotein, Coronavirus ; Vaccines ; Viral Envelope Proteins ; spike protein, SARS-CoV-2
Language	English
Publishing date	2022-04-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	80016-8
ISSN	1097-6868 ; 0002-9378
ISSN (online)	1097-6868
ISSN	0002-9378
DOI	10.1016/j.ajog.2022.04.009
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Article ; Online: Preserved recognition of Omicron Spike following COVID-19 mRNA vaccination in pregnancy

Bartsch, Yannic C / Atyeo, Caroline / Kang, Jaewon / Gray, Kathryn J / Edlow, Andrea G. / Alter, Galit

medRxiv

Abstract: Summary Background SARS-CoV-2 infection is associated with enhanced disease severity in pregnant women. Despite the potential of COVID-19 vaccines to reduce severe disease, vaccine uptake remained relatively low among pregnant women. Just as coordinated ... ...

Abstract	Summary Background SARS-CoV-2 infection is associated with enhanced disease severity in pregnant women. Despite the potential of COVID-19 vaccines to reduce severe disease, vaccine uptake remained relatively low among pregnant women. Just as coordinated messaging from the CDC and leading obstetrics organizations began to increase vaccine confidence in this vulnerable group, the evolution of SARS-CoV-2 variants of concerns (VOC) including the Omicron VOC raised new concerns about vaccine efficacy, given their ability to escape vaccine-induced neutralizing antibodies. Early data point to a milder disease course following omicron VOC infection in vaccinated individuals. Thus, these data suggest that alternate vaccine induced immunity, beyond neutralization, may continue to attenuate omicron disease, such as antibody-Fc-mediated activity. However, whether vaccine induced antibodies raised in pregnancy continue to bind and leverage Fc-receptors remains unclear. Methods VOC including Omicron receptor binding domain (RBD) or full Spike specific antibody isotype binding titers and FcγR binding were analyzed in pregnant women after the full dose regimen of either Pfizer/BioNtech BNT62b2 (n=10) or Moderna mRNA-1273 (n=10) vaccination using a multiplexing Luminex assay. Findings Comparable, albeit reduced, isotype recognition was observed to the Omicron Spike and receptor binding domain (RBD) following both vaccines. Yet, despite the near complete loss of Fc-receptor binding to the Omicron RBD, Fc-receptor binding was largely preserved to the Omicron Spike. Interpretation Reduced binding titer to the Omicron RBD aligns with observed loss of neutralizing activity. Despite the loss of neutralization, preserved Omicron Spike recognition and Fc-receptor binding potentially continues to attenuate disease severity in pregnant women. Funding NIH and the Bill and Melinda Gates Foundation
Keywords	covid19
Language	English
Publishing date	2022-01-02
Publisher	Cold Spring Harbor Laboratory Press
Document type	Article ; Online
DOI	10.1101/2022.01.01.22268615
Database	COVID19

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Article ; Online: Beta-spike-containing boosters induce robust and functional antibody responses to SARS-CoV-2 in macaques primed with distinct vaccines.

Deng, Yixiang / Atyeo, Caroline / Yuan, Dansu / Chicz, Taras M / Tibbitts, Timothy / Gorman, Matthew / Taylor, Sabian / Lecouturier, Valerie / Lauffenburger, Douglas A / Chicz, Roman M / Alter, Galit / McNamara, Ryan P

Cell reports

2023 Volume 42, Issue 11, Page(s) 113292

Abstract: The reduced effectiveness of COVID-19 vaccines due to the emergence of variants of concern (VOCs) necessitated the use of vaccine boosters to bolster protection against disease. However, it remains unclear how boosting expands protective breadth when ... ...

Abstract	The reduced effectiveness of COVID-19 vaccines due to the emergence of variants of concern (VOCs) necessitated the use of vaccine boosters to bolster protection against disease. However, it remains unclear how boosting expands protective breadth when primary vaccine platforms are distinct and how boosters containing VOC spike(s) broaden humoral responses. Here, we report that boosters composed of recombinant spike antigens of ancestral (prototype) and Beta VOCs elicit a robust, pan-VOC, and multi-functional humoral response in non-human primates largely independent of the primary vaccine series platform. Interestingly, Beta-spike-containing boosters stimulate immunoglobulin A (IgA) with a greater breadth of recognition in protein-primed recipients when administered with adjuvant system 03 (AS03). Our results highlight the utility of a component-based booster strategy for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) for broad humoral recognition, independent of primary vaccine series. This is of high global health importance given the heterogeneity of primary vaccination platforms distributed.
MeSH term(s)	Animals ; Humans ; SARS-CoV-2 ; COVID-19 Vaccines ; Macaca ; Antibody Formation ; COVID-19/prevention & control ; Vaccines ; Antibodies, Viral ; Antibodies, Neutralizing
Chemical Substances	COVID-19 Vaccines ; Vaccines ; Antibodies, Viral ; Antibodies, Neutralizing
Language	English
Publishing date	2023-10-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.113292
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Article ; Online: Selective functional antibody transfer into the breastmilk after SARS-CoV-2 infection.

Pullen, Krista M / Atyeo, Caroline / Collier, Ai-Ris Y / Gray, Kathryn J / Belfort, Mandy B / Lauffenburger, Douglas A / Edlow, Andrea G / Alter, Galit

Cell reports

2021 Volume 37, Issue 6, Page(s) 109959

Abstract: Antibody transfer via breastmilk represents an evolutionary strategy to boost immunity in early life. Although severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-specific antibodies have been observed in the breastmilk, the functional quality ... ...

Abstract	Antibody transfer via breastmilk represents an evolutionary strategy to boost immunity in early life. Although severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-specific antibodies have been observed in the breastmilk, the functional quality of these antibodies remains unclear. Here, we apply systems serology to characterize SARS-CoV-2-specific antibodies in maternal serum and breastmilk to compare the functional characteristics of antibodies in these fluids. Distinct SARS-CoV-2-specific antibody responses are observed in the serum and breastmilk of lactating individuals previously infected with SARS-CoV-2, with a more dominant transfer of immunoglobulin A (IgA) and IgM into breastmilk. Although IgGs are present in breastmilk, they are functionally attenuated. We observe preferential transfer of antibodies capable of eliciting neutrophil phagocytosis and neutralization compared to other functions, pointing to selective transfer of certain functional antibodies to breastmilk. These data highlight the preferential transfer of SARS-CoV-2-specific IgA and IgM to breastmilk, accompanied by select IgG subpopulations, positioned to create a non-pathologic but protective barrier against coronavirus disease 2019 (COVID-19).
MeSH term(s)	Antibodies, Viral/immunology ; Antibody Formation/immunology ; COVID-19/immunology ; Female ; Humans ; Immunoglobulin Isotypes/immunology ; Lactation/immunology ; Milk, Human/immunology ; Pregnancy ; Pregnancy Complications, Infectious/immunology ; SARS-CoV-2/immunology ; Spike Glycoprotein, Coronavirus/immunology
Chemical Substances	Antibodies, Viral ; Immunoglobulin Isotypes ; Spike Glycoprotein, Coronavirus
Language	English
Publishing date	2021-10-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.109959
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Article ; Online: Durability of Anti-Spike Antibodies in Infants After Maternal COVID-19 Vaccination or Natural Infection.

Shook, Lydia L / Atyeo, Caroline G / Yonker, Lael M / Fasano, Alessio / Gray, Kathryn J / Alter, Galit / Edlow, Andrea G

JAMA

2021 Volume 327, Issue 11, Page(s) 1087–1089

MeSH term(s)	Antibodies, Viral/blood ; COVID-19/blood ; COVID-19/immunology ; COVID-19 Vaccines ; Female ; Humans ; Infant ; Pregnancy ; Spike Glycoprotein, Coronavirus/immunology ; Time Factors
Chemical Substances	Antibodies, Viral ; COVID-19 Vaccines ; Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2021-12-31
Publishing country	United States
Document type	Letter ; Multicenter Study ; Research Support, N.I.H., Extramural
ZDB-ID	2958-0
ISSN	1538-3598 ; 0254-9077 ; 0002-9955 ; 0098-7484
ISSN (online)	1538-3598
ISSN	0254-9077 ; 0002-9955 ; 0098-7484
DOI	10.1001/jama.2022.1206
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Article ; Online: Beta-containing bivalent SARS-CoV-2 protein vaccine elicits durable broad neutralization in macaques and protection in hamsters.

Berry, Catherine / Pavot, Vincent / Anosova, Natalie G / Kishko, Michael / Li, Lu / Tibbitts, Tim / Raillard, Alice / Gautheron, Sylviane / Cummings, Sheila / Bangari, Dinesh S / Kar, Swagata / Atyeo, Caroline / Deng, Yixiang / Alter, Galit / Gutzeit, Cindy / Koutsoukos, Marguerite / Chicz, Roman M / Lecouturier, Valerie

Communications medicine

2023 Volume 3, Issue 1, Page(s) 75

Abstract: Background: Since the beginning of the COVID-19 pandemic, several variants of concern (VOC) have emerged for which there is evidence of an increase in transmissibility, more severe disease, and/or reduced vaccine effectiveness. Effective COVID-19 ... ...

Abstract	Background: Since the beginning of the COVID-19 pandemic, several variants of concern (VOC) have emerged for which there is evidence of an increase in transmissibility, more severe disease, and/or reduced vaccine effectiveness. Effective COVID-19 vaccine strategies are required to achieve broad protective immunity against current and future VOC. Methods: We conducted immunogenicity and challenge studies in macaques and hamsters using a bivalent recombinant vaccine formulation containing the SARS-CoV-2 prefusion-stabilized Spike trimers of the ancestral D614 and the variant Beta strains with AS03 adjuvant (CoV2 preS dTM-AS03) in a primary immunization setting. Results: We show that a primary immunization with the bivalent CoV2 preS dTM-AS03 elicits broader and durable (1 year) neutralizing antibody responses against VOC including Omicron BA.1 and BA.4/5, and SARS-CoV-1 as compared to the ancestral D614 or Beta variant monovalent vaccines in naïve non-human primates. In addition, the bivalent formulation confers protection against viral challenge with SARS-CoV-2 prototype D614G strain as well as Alpha and Beta variant strains in hamsters. Conclusions: Our findings demonstrate the potential of a Beta-containing bivalent CoV2 preS dTM-AS03 formulation to provide broad and durable immunogenicity, as well as protection against VOC in naïve populations.
Language	English
Publishing date	2023-05-26
Publishing country	England
Document type	Journal Article
ISSN	2730-664X
ISSN (online)	2730-664X
DOI	10.1038/s43856-023-00302-z
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Article ; Online: Humoral immunity to an endemic coronavirus is associated with postacute sequelae of COVID-19 in individuals with rheumatic diseases.

Herman, Jonathan D / Atyeo, Caroline / Zur, Yonatan / Cook, Claire E / Patel, Naomi J / Vanni, Kathleen M / Kowalski, Emily N / Qian, Grace / Srivatsan, Shruthi / Shadick, Nancy A / Rao, Deepak A / Kellman, Benjamin / Mann, Colin J / Lauffenburger, Douglas / Wallace, Zachary S / Sparks, Jeffrey A / Alter, Galit

Science translational medicine

2023 Volume 15, Issue 712, Page(s) eadf6598

Abstract: Beyond the acute illness caused by severe acute respiratory coronavirus 2 (SARS-CoV-2) infection, about one-fifth of infections result in long-term persistence of symptoms despite the apparent clearance of infection. Insights into the mechanisms that ... ...

Abstract	Beyond the acute illness caused by severe acute respiratory coronavirus 2 (SARS-CoV-2) infection, about one-fifth of infections result in long-term persistence of symptoms despite the apparent clearance of infection. Insights into the mechanisms that underlie postacute sequelae of COVID-19 (PASC) will be critical for the prevention and clinical management of long-term complications of COVID-19. Several hypotheses have been proposed that may account for the development of PASC, including persistence of virus and dysregulation of immune responses. Among the immunological changes noted in PASC, alterations in humoral immunity have been observed in some patient subsets. To begin to determine whether SARS-CoV-2- or other pathogen-specific humoral immune responses evolve uniquely in PASC, we performed comprehensive antibody profiling against SARS-CoV-2, a panel of endemic pathogens, and a panel of routine vaccine antigens using systems serology in two cohorts of patients with preexisting systemic autoimmune rheumatic disease (SARD) who either developed or did not develop PASC. A distinct qualitative shift observed in Fcγ receptor (FcγR) binding was observed in individuals with PASC. Specifically, individuals with PASC harbored weaker FcγR-binding anti-SARS-CoV-2 antibodies and stronger FcγR-binding antibody responses against the endemic coronavirus OC43. Individuals with PASC developed an OC43 S2-specific antibody response with stronger FcγR binding, linked to cross-reactivity across SARS-CoV-2 and common coronaviruses. These findings identify previous coronavirus imprinting as a potential marker for the development of PASC in individuals with SARDs.
MeSH term(s)	Immunity, Humoral ; Rheumatic Diseases/complications ; Rheumatic Diseases/immunology ; SARS-CoV-2/immunology ; Humans ; Male ; Female ; Middle Aged ; Aged ; Post-Acute COVID-19 Syndrome/complications ; Post-Acute COVID-19 Syndrome/immunology ; Endemic Diseases ; Receptors, Fc/metabolism ; Antibodies, Viral/blood ; Antibodies, Viral/immunology ; Spike Glycoprotein, Coronavirus/immunology
Chemical Substances	Receptors, Fc ; Antibodies, Viral ; spike protein, SARS-CoV-2 ; Spike Glycoprotein, Coronavirus
Language	English
Publishing date	2023-09-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2518854-9
ISSN	1946-6242 ; 1946-6234
ISSN (online)	1946-6242
ISSN	1946-6234
DOI	10.1126/scitranslmed.adf6598
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Article: Lectin Fingerprinting Distinguishes Antibody Neutralization in SARS-CoV-2.

Wuo, Michael G / Dugan, Amanda E / Halim, Melanie / Hauser, Blake M / Feldman, Jared / Caradonna, Timothy M / Zhang, Shuting / Pepi, Lauren E / Atyeo, Caroline / Fischinger, Stephanie / Alter, Galit / Garcia-Beltran, Wilfredo F / Azadi, Parastoo / Hung, Deb / Schmidt, Aaron G / Kiessling, Laura L

ACS central science

2023 Volume 9, Issue 5, Page(s) 947–956

Abstract: Enveloped viruses co-opt host glycosylation pathways to decorate their surface proteins. As viruses evolve, emerging strains can modify their glycosylation patterns to influence host interactions and subvert immune recognition. Still, changes in viral ... ...

Abstract	Enveloped viruses co-opt host glycosylation pathways to decorate their surface proteins. As viruses evolve, emerging strains can modify their glycosylation patterns to influence host interactions and subvert immune recognition. Still, changes in viral glycosylation or their impact on antibody protection cannot be predicted from genomic sequences alone. Using the highly glycosylated SARS-CoV-2 Spike protein as a model system, we present a lectin fingerprinting method that rapidly reports on changes in variant glycosylation state, which are linked to antibody neutralization. In the presence of antibodies or convalescent and vaccinated patient sera, unique lectin fingerprints emerge that distinguish neutralizing versus non-neutralizing antibodies. This information could not be inferred from direct binding interactions between antibodies and the Spike receptor-binding domain (RBD) binding data alone. Comparative glycoproteomics of the Spike RBD of wild-type (Wuhan-Hu-1) and Delta (B.1.617.2) variants reveal O-glycosylation differences as a key determinant of immune recognition differences. These data underscore the interplay between viral glycosylation and immune recognition and reveal lectin fingerprinting to be a rapid, sensitive, and high-throughput assay to distinguish the neutralization potential of antibodies that target critical viral glycoproteins.
Language	English
Publishing date	2023-05-10
Publishing country	United States
Document type	Journal Article
ISSN	2374-7943
ISSN	2374-7943
DOI	10.1021/acscentsci.2c01471
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