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Single cell analysis of blood mononuclear cells stimulated through CD3 and CD28 shows collateral activation of B and NK cells and demise of monocytes

View ORCID ProfileNathan Lawlor, Djamel Nehar-Belaid, Jessica D.S. Grassmann, Marlon Stoeckius, Peter Smibert, Michael L. Stitzel, Virginia Pascual, Jacques Banchereau, Adam Williams, Duygu Ucar
doi: https://doi.org/10.1101/2020.12.23.424147
Nathan Lawlor
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
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  • ORCID record for Nathan Lawlor
Djamel Nehar-Belaid
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
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Jessica D.S. Grassmann
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
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Marlon Stoeckius
210X Genomics, Stockholm, Sweden
3New York Genome Center, New York, NY 10013, USA
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Peter Smibert
3New York Genome Center, New York, NY 10013, USA
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Michael L. Stitzel
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
4Institute of Systems Genomics, University of Connecticut, Farmington, CT 06032, USA
5Department of Genetics and Genome Sciences, University of Connecticut, Farmington, CT 06032, USA
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Virginia Pascual
6Ronay Menschel Professor of Pediatrics, Drukier Institute, Weill Cornell Medicine, New York, NY 10065, USA
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Jacques Banchereau
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
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  • For correspondence: Jacques.Banchereau@jax.org adam.williams@jax.org duygu.ucar@jax.org
Adam Williams
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
4Institute of Systems Genomics, University of Connecticut, Farmington, CT 06032, USA
5Department of Genetics and Genome Sciences, University of Connecticut, Farmington, CT 06032, USA
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  • For correspondence: Jacques.Banchereau@jax.org adam.williams@jax.org duygu.ucar@jax.org
Duygu Ucar
1The Jackson Laboratory for Genomic Medicine, Farmington, CT, 06030, USA
4Institute of Systems Genomics, University of Connecticut, Farmington, CT 06032, USA
5Department of Genetics and Genome Sciences, University of Connecticut, Farmington, CT 06032, USA
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  • For correspondence: Jacques.Banchereau@jax.org adam.williams@jax.org duygu.ucar@jax.org
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Abstract

Immune cell activation assays have been widely used for immune monitoring and for understanding disease mechanisms. However, these assays are typically limited in scope. A holistic study of circulating immune cell responses to different activators is lacking. Here we developed a cost-effective high-throughput multiplexed single-cell RNA-seq combined with epitope tagging (CITE-seq) to determine how classic activators of T cells (anti-CD3 coupled with anti-CD28) or monocytes (LPS) alter the cell composition and transcriptional profiles of peripheral blood mononuclear cells (PBMCs) from healthy human donors. Anti-CD3/CD28 treatment activated all classes of lymphocytes either directly (T cells) or indirectly (B and NK cells) but reduced monocyte numbers. Activated T and NK cells expressed senescence and effector molecules, whereas activated B cells transcriptionally resembled autoimmune disease- or age-associated B cells (e.g., CD11c, T-bet). In contrast, LPS specifically targeted monocytes and induced two main states: early activation characterized by the expression of chemoattractants and a later pro-inflammatory state characterized by expression of effector molecules. These data provide a foundation for future immune activation studies with single cell technologies (https://czi-pbmc-cite-seq.jax.org/).

Figure

Competing Interest Statement

The authors have declared no competing interest.

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Posted December 24, 2020.
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Single cell analysis of blood mononuclear cells stimulated through CD3 and CD28 shows collateral activation of B and NK cells and demise of monocytes
Nathan Lawlor, Djamel Nehar-Belaid, Jessica D.S. Grassmann, Marlon Stoeckius, Peter Smibert, Michael L. Stitzel, Virginia Pascual, Jacques Banchereau, Adam Williams, Duygu Ucar
bioRxiv 2020.12.23.424147; doi: https://doi.org/10.1101/2020.12.23.424147
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Single cell analysis of blood mononuclear cells stimulated through CD3 and CD28 shows collateral activation of B and NK cells and demise of monocytes
Nathan Lawlor, Djamel Nehar-Belaid, Jessica D.S. Grassmann, Marlon Stoeckius, Peter Smibert, Michael L. Stitzel, Virginia Pascual, Jacques Banchereau, Adam Williams, Duygu Ucar
bioRxiv 2020.12.23.424147; doi: https://doi.org/10.1101/2020.12.23.424147

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