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Prenatal SARS-CoV-2 infection alters postpartum human milk-derived extracellular vesicles

View ORCID ProfileSomchai Chutipongtanate, Hatice Cetinkaya, Xiang Zhang, Damaris Kuhnell, Desirée Benefield, Wendy Haffey, Michael Wyder, Richa Patel, Shannon C. Conrey, Allison R. Burrell, Scott Langevin, View ORCID ProfileLaurie Nommsen-Rivers, View ORCID ProfileDavid S. Newburg, View ORCID ProfileKenneth D. Greis, Mary A. Staat, View ORCID ProfileArdythe L. Morrow
doi: https://doi.org/10.1101/2023.06.01.543234
Somchai Chutipongtanate
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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  • ORCID record for Somchai Chutipongtanate
  • For correspondence: chutipsi@ucmail.uc.edu morrowa@ucmail.uc.edu
Hatice Cetinkaya
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Xiang Zhang
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Damaris Kuhnell
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Desirée Benefield
2Department of Molecular Cellular Biosciences, Center for Advanced Structural Biology, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Wendy Haffey
3Department of Cancer Biology, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Michael Wyder
3Department of Cancer Biology, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Richa Patel
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Shannon C. Conrey
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Allison R. Burrell
4Department of Infectious Disease, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45267 USA
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Scott Langevin
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Laurie Nommsen-Rivers
5Department of Rehabilitation, Exercise, and Nutrition, University of Cincinnati College of Allied Health Sciences, Cincinnati, OH 45267 USA
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  • ORCID record for Laurie Nommsen-Rivers
David S. Newburg
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Kenneth D. Greis
3Department of Cancer Biology, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
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Mary A. Staat
4Department of Infectious Disease, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45267 USA
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Ardythe L. Morrow
1Department of Environmental and Public Health Sciences, University of Cincinnati College of Medicine, Cincinnati, OH 45267 USA
4Department of Infectious Disease, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45267 USA
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  • For correspondence: chutipsi@ucmail.uc.edu morrowa@ucmail.uc.edu
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ABSTRACT

Human milk-derived extracellular vesicles (HMEVs) are crucial functional components in breast milk, contributing to infant health and development. Maternal conditions could affect HMEV cargos; however, the impact of SARS-CoV-2 infection on HMEVs remains unknown. This study evaluated the influence of SARS-CoV-2 infection during pregnancy on postpartum HMEV molecules. Milk samples (9 prenatal SARS-CoV-2 vs. 9 controls) were retrieved from the IMPRINT birth cohort. After defatting and casein micelle disaggregation, 1 mL milk was subjected to a sequential process of centrifugation, ultrafiltration, and qEV-size exclusion chromatography. Particle and protein characterizations were performed following the MISEV2018 guidelines. EV lysates were analyzed through proteomics and miRNA sequencing, while the intact EVs were biotinylated for surfaceomic analysis. Multi-Omics was employed to predict HMEV functions associated with prenatal SARS-CoV-2 infection. Demographic data between the prenatal SARS-CoV-2 and control groups were similar. The median duration from maternal SARS-CoV-2 test positivity to milk collection was 3 months (range: 1-6 months). Transmission electron microscopy showed the cup-shaped nanoparticles. Nanoparticle tracking analysis demonstrated particle diameters of <200 nm and yields of >1e11 particles from 1 mL milk. Western immunoblots detected ALIX, CD9 and HSP70, supporting the presence of HMEVs in the isolates. Thousands of HMEV cargos and hundreds of surface proteins were identified and compared. Multi-Omics predicted that mothers with prenatal SARS-CoV-2 infection produced HMEVs with enhanced functionalities involving metabolic reprogramming and mucosal tissue development, while mitigating inflammation and lower EV transmigration potential. Our findings suggest that SARS-CoV-2 infection during pregnancy boosts mucosal site-specific functions of HMEVs, potentially protecting infants against viral infections. Further prospective studies should be pursued to reevaluate the short- and long-term benefits of breastfeeding in the post-COVID era.

Competing Interest Statement

The authors have declared no competing interest.

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Prenatal SARS-CoV-2 infection alters postpartum human milk-derived extracellular vesicles
Somchai Chutipongtanate, Hatice Cetinkaya, Xiang Zhang, Damaris Kuhnell, Desirée Benefield, Wendy Haffey, Michael Wyder, Richa Patel, Shannon C. Conrey, Allison R. Burrell, Scott Langevin, Laurie Nommsen-Rivers, David S. Newburg, Kenneth D. Greis, Mary A. Staat, Ardythe L. Morrow
bioRxiv 2023.06.01.543234; doi: https://doi.org/10.1101/2023.06.01.543234
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Prenatal SARS-CoV-2 infection alters postpartum human milk-derived extracellular vesicles
Somchai Chutipongtanate, Hatice Cetinkaya, Xiang Zhang, Damaris Kuhnell, Desirée Benefield, Wendy Haffey, Michael Wyder, Richa Patel, Shannon C. Conrey, Allison R. Burrell, Scott Langevin, Laurie Nommsen-Rivers, David S. Newburg, Kenneth D. Greis, Mary A. Staat, Ardythe L. Morrow
bioRxiv 2023.06.01.543234; doi: https://doi.org/10.1101/2023.06.01.543234

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