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Article ; Online: Comparative analysis of cell-cell communication at single-cell resolution.

Wilk, Aaron J / Shalek, Alex K / Holmes, Susan / Blish, Catherine A

2023 Volume 42, Issue 3, Page(s) 470–483

Abstract: Inference of cell-cell communication from single-cell RNA sequencing data is a powerful technique to uncover intercellular communication pathways, yet existing methods perform this analysis at the level of the cell type or cluster, discarding single-cell- ...

Abstract	Inference of cell-cell communication from single-cell RNA sequencing data is a powerful technique to uncover intercellular communication pathways, yet existing methods perform this analysis at the level of the cell type or cluster, discarding single-cell-level information. Here we present Scriabin, a flexible and scalable framework for comparative analysis of cell-cell communication at single-cell resolution that is performed without cell aggregation or downsampling. We use multiple published atlas-scale datasets, genetic perturbation screens and direct experimental validation to show that Scriabin accurately recovers expected cell-cell communication edges and identifies communication networks that can be obscured by agglomerative methods. Additionally, we use spatial transcriptomic data to show that Scriabin can uncover spatial features of interaction from dissociated data alone. Finally, we demonstrate applications to longitudinal datasets to follow communication pathways operating between timepoints. Our approach represents a broadly applicable strategy to reveal the full structure of niche-phenotype relationships in health and disease.
MeSH term(s)	Cell Communication/genetics ; Gene Expression Profiling ; Transcriptome ; Single-Cell Analysis
Language	English
Publishing date	2023-05-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	1311932-1
ISSN	1546-1696 ; 1087-0156
ISSN (online)	1546-1696
ISSN	1087-0156
DOI	10.1038/s41587-023-01782-z
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Article: Comparative analysis of cell-cell communication at single-cell resolution.

Wilk, Aaron J / Shalek, Alex K / Holmes, Susan / Blish, Catherine A

bioRxiv : the preprint server for biology

2022

Abstract: Inference of cell-cell communication (CCC) from single-cell RNA-sequencing data is a powerful technique to uncover putative axes of multicellular coordination, yet existing methods perform this analysis at the level of the cell type or cluster, ... ...

Abstract	Inference of cell-cell communication (CCC) from single-cell RNA-sequencing data is a powerful technique to uncover putative axes of multicellular coordination, yet existing methods perform this analysis at the level of the cell type or cluster, discarding single-cell level information. Here we present Scriabin â€" a flexible and scalable framework for comparative analysis of CCC at single-cell resolution. We leverage multiple published datasets to show that Scriabin recovers expected CCC edges and use spatial transcriptomic data, genetic perturbation screens, and direct experimental manipulation of receptor-ligand interactions to validate that the recovered edges are biologically meaningful. We then apply Scriabin to uncover co-expressed programs of CCC from atlas-scale datasets, validating known communication pathways required for maintaining the intestinal stem cell niche and revealing species-specific communication pathways. Finally, we utilize single-cell communication networks calculated using Scriabin to follow communication pathways that operate between timepoints in longitudinal datasets, highlighting bystander cells as important initiators of inflammatory reactions in acute SARS-CoV-2 infection. Our approach represents a broadly applicable strategy to leverage single-cell resolution data maximally toward uncovering CCC circuitry and rich niche-phenotype relationships in health and disease.
Language	English
Publishing date	2022-07-25
Publishing country	United States
Document type	Preprint
DOI	10.1101/2022.02.04.479209
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Article ; Online: Single-cell RNA-seq methods to interrogate virus-host interactions

Ratnasiri, Kalani / Wilk, Aaron J. / Lee, Madeline J. / Khatri, Purvesh / Blish, Catherine A.

Semin Immunopathol. 2023 Jan., v. 45, no. 1, p. 71-89

2023 , Page(s) 71–89

Abstract: The twenty-first century has seen the emergence of many epidemic and pandemic viruses, with the most recent being the SARS-CoV-2-driven COVID-19 pandemic. As obligate intracellular parasites, viruses rely on host cells to replicate and produce progeny, ... ...

Abstract	The twenty-first century has seen the emergence of many epidemic and pandemic viruses, with the most recent being the SARS-CoV-2-driven COVID-19 pandemic. As obligate intracellular parasites, viruses rely on host cells to replicate and produce progeny, resulting in complex virus and host dynamics during an infection. Single-cell RNA sequencing (scRNA-seq), by enabling broad and simultaneous profiling of both host and virus transcripts, represents a powerful technology to unravel the delicate balance between host and virus. In this review, we summarize technological and methodological advances in scRNA-seq and their applications to antiviral immunity. We highlight key scRNA-seq applications that have enabled the understanding of viral genomic and host response heterogeneity, differential responses of infected versus bystander cells, and intercellular communication networks. We expect further development of scRNA-seq technologies and analytical methods, combined with measurements of additional multi-omic modalities and increased availability of publicly accessible scRNA-seq datasets, to enable a better understanding of viral pathogenesis and enhance the development of antiviral therapeutics strategies.
Keywords	COVID-19 infection ; RNA ; cell communication ; data collection ; genomics ; immunity ; pandemic ; pathogenesis ; progeny ; sequence analysis ; therapeutics ; viruses
Language	English
Dates of publication	2023-01
Size	p. 71-89
Publishing place	Springer Berlin Heidelberg
Document type	Article ; Online
Note	Review
ZDB-ID	2316828-6
ISSN	1863-2300 ; 1863-2297
ISSN (online)	1863-2300
ISSN	1863-2297
DOI	10.1007/s00281-022-00972-2
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Article ; Online: Diversification of human NK cells: Lessons from deep profiling.

Wilk, Aaron J / Blish, Catherine A

Journal of leukocyte biology

2018 Volume 103, Issue 4, Page(s) 629–641

Abstract: NK cells are innate lymphocytes with important roles in immunoregulation, immunosurveillance, and cytokine production. Originally defined on the functional basis of their "natural" ability to lyse tumor targets and thought to be a relatively homogeneous ... ...

Abstract	NK cells are innate lymphocytes with important roles in immunoregulation, immunosurveillance, and cytokine production. Originally defined on the functional basis of their "natural" ability to lyse tumor targets and thought to be a relatively homogeneous group of lymphocytes, NK cells possess a remarkable degree of phenotypic and functional diversity due to the combinatorial expression of an array of activating and inhibitory receptors. Diversification of NK cells is multifaceted: mechanisms of NK cell education that promote self-tolerance result in a heterogeneous repertoire that further diversifies upon encounters with viral pathogens. Here, we review the genetic, developmental, and environmental sources of NK cell diversity with a particular focus on deep profiling and single-cell technologies that will enable a more thorough and accurate dissection of this intricate and poorly understood lymphocyte lineage.
MeSH term(s)	Animals ; Environment ; Gene Expression Profiling ; Gene Expression Regulation ; Humans ; Immunologic Memory ; Killer Cells, Natural/cytology ; Killer Cells, Natural/immunology ; Killer Cells, Natural/metabolism
Language	English
Publishing date	2018-01-19
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	605722-6
ISSN	1938-3673 ; 0741-5400
ISSN (online)	1938-3673
ISSN	0741-5400
DOI	10.1002/JLB.6RI0917-390R
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Article ; Online: Single-cell RNA-seq methods to interrogate virus-host interactions.

Ratnasiri, Kalani / Wilk, Aaron J / Lee, Madeline J / Khatri, Purvesh / Blish, Catherine A

Seminars in immunopathology

2022 Volume 45, Issue 1, Page(s) 71–89

Abstract	The twenty-first century has seen the emergence of many epidemic and pandemic viruses, with the most recent being the SARS-CoV-2-driven COVID-19 pandemic. As obligate intracellular parasites, viruses rely on host cells to replicate and produce progeny, resulting in complex virus and host dynamics during an infection. Single-cell RNA sequencing (scRNA-seq), by enabling broad and simultaneous profiling of both host and virus transcripts, represents a powerful technology to unravel the delicate balance between host and virus. In this review, we summarize technological and methodological advances in scRNA-seq and their applications to antiviral immunity. We highlight key scRNA-seq applications that have enabled the understanding of viral genomic and host response heterogeneity, differential responses of infected versus bystander cells, and intercellular communication networks. We expect further development of scRNA-seq technologies and analytical methods, combined with measurements of additional multi-omic modalities and increased availability of publicly accessible scRNA-seq datasets, to enable a better understanding of viral pathogenesis and enhance the development of antiviral therapeutics strategies.
MeSH term(s)	Humans ; Sequence Analysis, RNA/methods ; Host Microbial Interactions ; Pandemics ; Single-Cell Gene Expression Analysis ; COVID-19 ; SARS-CoV-2 ; Antiviral Agents ; Gene Expression Profiling
Chemical Substances	Antiviral Agents
Language	English
Publishing date	2022-11-21
Publishing country	Germany
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2316828-6
ISSN	1863-2300 ; 1863-2297
ISSN (online)	1863-2300
ISSN	1863-2297
DOI	10.1007/s00281-022-00972-2
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Article ; Online: Pro-inflammatory feedback loops define immune responses to pathogenic Lentivirus infection.

Wilk, Aaron J / Marceau, Joshua O / Kazer, Samuel W / Fleming, Ira / Miao, Vincent N / Galvez-Reyes, Jennyfer / Kimata, Jason T / Shalek, Alex K / Holmes, Susan / Overbaugh, Julie / Blish, Catherine A

Genome medicine

2024 Volume 16, Issue 1, Page(s) 24

Abstract: Background: The Lentivirus human immunodeficiency virus (HIV) causes chronic inflammation and AIDS in humans, with variable rates of disease progression between individuals driven by both host and viral factors. Similarly, simian lentiviruses vary in ... ...

Abstract	Background: The Lentivirus human immunodeficiency virus (HIV) causes chronic inflammation and AIDS in humans, with variable rates of disease progression between individuals driven by both host and viral factors. Similarly, simian lentiviruses vary in their pathogenicity based on characteristics of both the host species and the virus strain, yet the immune underpinnings that drive differential Lentivirus pathogenicity remain incompletely understood. Methods: We profile immune responses in a unique model of differential lentiviral pathogenicity where pig-tailed macaques are infected with highly genetically similar variants of SIV that differ in virulence. We apply longitudinal single-cell transcriptomics to this cohort, along with single-cell resolution cell-cell communication techniques, to understand the immune mechanisms underlying lentiviral pathogenicity. Results: Compared to a minimally pathogenic lentiviral variant, infection with a highly pathogenic variant results in a more delayed, broad, and sustained activation of inflammatory pathways, including an extensive global interferon signature. Conversely, individual cells infected with highly pathogenic Lentivirus upregulated fewer interferon-stimulated genes at a lower magnitude, indicating that highly pathogenic Lentivirus has evolved to partially escape from interferon responses. Further, we identify CXCL10 and CXCL16 as important molecular drivers of inflammatory pathways specifically in response to highly pathogenic Lentivirus infection. Immune responses to highly pathogenic Lentivirus infection are characterized by amplifying regulatory circuits of pro-inflammatory cytokines with dense longitudinal connectivity. Conclusions: Our work presents a model of lentiviral pathogenicity where failures in early viral control mechanisms lead to delayed, sustained, and amplifying pro-inflammatory circuits, which in turn drives disease progression.
MeSH term(s)	Animals ; Humans ; Simian Acquired Immunodeficiency Syndrome ; Simian Immunodeficiency Virus/genetics ; Feedback ; Lentivirus Infections ; Disease Progression ; Immunity ; Interferons
Chemical Substances	Interferons (9008-11-1)
Language	English
Publishing date	2024-02-05
Publishing country	England
Document type	Journal Article
ZDB-ID	2484394-5
ISSN	1756-994X ; 1756-994X
ISSN (online)	1756-994X
ISSN	1756-994X
DOI	10.1186/s13073-024-01290-y
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Article ; Online: NK Cell-Monocyte Cross-talk Underlies NK Cell Activation in Severe COVID-19.

Lee, Madeline J / de Los Rios Kobara, Izumi / Barnard, Trisha R / Vales Torres, Xariana / Tobin, Nicole H / Ferbas, Kathie G / Rimoin, Anne W / Yang, Otto O / Aldrovandi, Grace M / Wilk, Aaron J / Fulcher, Jennifer A / Blish, Catherine A

Journal of immunology (Baltimore, Md. : 1950)

2024

Abstract: NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, ...

Abstract	NK cells in the peripheral blood of severe COVID-19 patients exhibit a unique profile characterized by activation and dysfunction. Previous studies have identified soluble factors, including type I IFN and TGF-β, that underlie this dysregulation. However, the role of cell-cell interactions in modulating NK cell function during COVID-19 remains unclear. To address this question, we combined cell-cell communication analysis on existing single-cell RNA sequencing data with in vitro primary cell coculture experiments to dissect the mechanisms underlying NK cell dysfunction in COVID-19. We found that NK cells are predicted to interact most strongly with monocytes and that this occurs via both soluble factors and direct interactions. To validate these findings, we performed in vitro cocultures in which NK cells from healthy human donors were incubated with monocytes from COVID-19+ or healthy donors. Coculture of healthy NK cells with monocytes from COVID-19 patients recapitulated aspects of the NK cell phenotype observed in severe COVID-19, including decreased expression of NKG2D, increased expression of activation markers, and increased proliferation. When these experiments were performed in a Transwell setting, we found that only CD56bright CD16- NK cells were activated in the presence of severe COVID-19 patient monocytes. O-link analysis of supernatants from Transwell cocultures revealed that cultures containing severe COVID-19 patient monocytes had significantly elevated levels of proinflammatory cytokines and chemokines, as well as TGF-β. Collectively, these results demonstrate that interactions between NK cells and monocytes in the peripheral blood of COVID-19 patients contribute to NK cell activation and dysfunction in severe COVID-19.
Language	English
Publishing date	2024-04-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2300731
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Article: Disrupted memory T cell expansion in HIV-exposed uninfected infants is preceded by premature skewing of T cell receptor clonality.

Dzanibe, Sonwabile / Wilk, Aaron J / Canny, Susan / Ranganath, Thanmayi / Alinde, Berenice / Rubelt, Florian / Huang, Huang / Davis, Mark M / Holmes, Susan / Jaspan, Heather B / Blish, Catherine A / Gray, Clive M

bioRxiv : the preprint server for biology

2023

Abstract: While preventing vertical HIV transmission has been very successful, the increasing number of HIV-exposed uninfected infants (iHEU) experience an elevated risk to infections compared to HIV-unexposed and uninfected infants (iHUU). Immune developmental ... ...

Abstract	While preventing vertical HIV transmission has been very successful, the increasing number of HIV-exposed uninfected infants (iHEU) experience an elevated risk to infections compared to HIV-unexposed and uninfected infants (iHUU). Immune developmental differences between iHEU and iHUU remains poorly understood and here we present a longitudinal multimodal analysis of infant immune ontogeny that highlights the impact of HIV/ARV exposure. Using mass cytometry, we show alterations and differences in the emergence of NK cell populations and T cell memory differentiation between iHEU and iHUU. Specific NK cells observed at birth were also predictive of acellular pertussis and rotavirus vaccine-induced IgG and IgA responses, respectively, at 3 and 9 months of life. T cell receptor Vβ clonotypic diversity was significantly and persistently lower in iHEU preceding the expansion of T cell memory. Our findings show that HIV/ARV exposure disrupts innate and adaptive immunity from birth which may underlie relative vulnerability to infections.
Language	English
Publishing date	2023-05-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.19.540713
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Article ; Online: Interstitial macrophages are a focus of viral takeover and inflammation in COVID-19 initiation in human lung.

Wu, Timothy Ting-Hsuan / Travaglini, Kyle J / Rustagi, Arjun / Xu, Duo / Zhang, Yue / Andronov, Leonid / Jang, SoRi / Gillich, Astrid / Dehghannasiri, Roozbeh / Martínez-Colón, Giovanny J / Beck, Aimee / Liu, Daniel Dan / Wilk, Aaron J / Morri, Maurizio / Trope, Winston L / Bierman, Rob / Weissman, Irving L / Shrager, Joseph B / Quake, Stephen R /

Kuo, Christin S / Salzman, Julia / Moerner, W E / Kim, Peter S / Blish, Catherine A / Krasnow, Mark A

The Journal of experimental medicine

2024 Volume 221, Issue 6

Abstract: Early stages of deadly respiratory diseases including COVID-19 are challenging to elucidate in humans. Here, we define cellular tropism and transcriptomic effects of SARS-CoV-2 virus by productively infecting healthy human lung tissue and using scRNA-seq ...

Abstract	Early stages of deadly respiratory diseases including COVID-19 are challenging to elucidate in humans. Here, we define cellular tropism and transcriptomic effects of SARS-CoV-2 virus by productively infecting healthy human lung tissue and using scRNA-seq to reconstruct the transcriptional program in "infection pseudotime" for individual lung cell types. SARS-CoV-2 predominantly infected activated interstitial macrophages (IMs), which can accumulate thousands of viral RNA molecules, taking over 60% of the cell transcriptome and forming dense viral RNA bodies while inducing host profibrotic (TGFB1, SPP1) and inflammatory (early interferon response, CCL2/7/8/13, CXCL10, and IL6/10) programs and destroying host cell architecture. Infected alveolar macrophages (AMs) showed none of these extreme responses. Spike-dependent viral entry into AMs used ACE2 and Sialoadhesin/CD169, whereas IM entry used DC-SIGN/CD209. These results identify activated IMs as a prominent site of viral takeover, the focus of inflammation and fibrosis, and suggest targeting CD209 to prevent early pathology in COVID-19 pneumonia. This approach can be generalized to any human lung infection and to evaluate therapeutics.
MeSH term(s)	Humans ; COVID-19 ; SARS-CoV-2 ; Macrophages ; Inflammation ; RNA, Viral ; Lung
Chemical Substances	RNA, Viral
Language	English
Publishing date	2024-04-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20232192
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Article ; Online: Charge-altering releasable transporters enable phenotypic manipulation of natural killer cells for cancer immunotherapy.

Wilk, Aaron J / Weidenbacher, Nancy Lynn-Benner / Vergara, Rosemary / Haabeth, Ole A W / Levy, Ronald / Waymouth, Robert M / Wender, Paul A / Blish, Catherine A

Blood advances

2020 Volume 4, Issue 17, Page(s) 4244–4255

Abstract: Chimeric antigen receptor (CAR) natural killer (NK) cells are an emerging cell therapy with promising results in oncology trials. However, primary human NK cells are difficult to transfect, hampering both mechanistic studies and clinical applications of ... ...

Abstract	Chimeric antigen receptor (CAR) natural killer (NK) cells are an emerging cell therapy with promising results in oncology trials. However, primary human NK cells are difficult to transfect, hampering both mechanistic studies and clinical applications of NK cells. Currently, NK cell CAR modification relies on viral vectors or cell activation. The former raises cost and tolerability issues, while the latter alters NK cell biology. Here, we report that readily synthesized and inexpensive nonviral charge-altering releasable transporters (CARTs) efficiently transfect primary human NK cells with messenger RNA without relying on NK cell activation. Compared with electroporation, CARTs transfect NK cells more efficiently, better preserve cell viability, and cause minimal reconfiguration of NK cell phenotype and function. We use CARTs to generate cytotoxic primary anti-CD19 CAR NK cells, demonstrating this technology can drive clinical applications of NK cells. To our knowledge, CARTs represent the first efficacious transfection technique for resting primary human NK cells that preserves NK cell phenotype and can enable new biological discoveries and therapeutic applications of this understudied lymphocyte subset.
MeSH term(s)	Cell Line, Tumor ; Humans ; Immunotherapy ; Killer Cells, Natural ; Neoplasms/therapy ; Phenotype ; Receptors, Chimeric Antigen/genetics
Chemical Substances	Receptors, Chimeric Antigen
Language	English
Publishing date	2020-08-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2915908-8
ISSN	2473-9537 ; 2473-9529
ISSN (online)	2473-9537
ISSN	2473-9529
DOI	10.1182/bloodadvances.2020002355
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