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Article ; Online: Single-cell profiling to transform immunotherapy usage and target discovery in immune-mediated inflammatory diseases.

Chapelle, Nicolas / Fantou, Aurelie / Marron, Thomas / Kenigsberg, Ephraim / Merad, Miriam / Martin, Jerome C

2022 Volume 13, Page(s) 1006944

Abstract: Immunotherapy drugs are transforming the clinical care landscape of major human diseases from cancer, to inflammatory diseases, cardiovascular diseases, neurodegenerative diseases and even aging. In polygenic immune-mediated inflammatory diseases (IMIDs), ...

Abstract	Immunotherapy drugs are transforming the clinical care landscape of major human diseases from cancer, to inflammatory diseases, cardiovascular diseases, neurodegenerative diseases and even aging. In polygenic immune-mediated inflammatory diseases (IMIDs), the clinical benefits of immunotherapy have nevertheless remained limited to a subset of patients. Yet the identification of new actionable molecular candidates has remained challenging, and the use of standard of care imaging and/or histological diagnostic assays has failed to stratify potential responders from non-responders to biotherapies already available. We argue that these limitations partly stem from a poor understanding of disease pathophysiology and insufficient characterization of the roles assumed by candidate targets during disease initiation, progression and treatment. By transforming the resolution and scale of tissue cell mapping, high-resolution profiling strategies offer unprecedented opportunities to the understanding of immunopathogenic events in human IMID lesions. Here we discuss the potential for single-cell technologies to reveal relevant pathogenic cellular programs in IMIDs and to enhance patient stratification to guide biotherapy eligibility and clinical trial design.
MeSH term(s)	Humans ; Immunotherapy ; Immunologic Factors ; Immunomodulating Agents ; Aging ; Biological Assay
Chemical Substances	Immunologic Factors ; Immunomodulating Agents
Language	English
Publishing date	2022-11-07
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.1006944
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Article ; Online: Drosophila functional elements are embedded in structurally constrained sequences.

Kenigsberg, Ephraim / Tanay, Amos

PLoS genetics

2013 Volume 9, Issue 5, Page(s) e1003512

Abstract: Modern functional genomics uncovered numerous functional elements in metazoan genomes. Nevertheless, only a small fraction of the typical non-exonic genome contains elements that code for function directly. On the other hand, a much larger fraction of ... ...

Abstract	Modern functional genomics uncovered numerous functional elements in metazoan genomes. Nevertheless, only a small fraction of the typical non-exonic genome contains elements that code for function directly. On the other hand, a much larger fraction of the genome is associated with significant evolutionary constraints, suggesting that much of the non-exonic genome is weakly functional. Here we show that in flies, local (30-70 bp) conserved sequence elements that are associated with multiple regulatory functions serve as focal points to a pattern of punctuated regional increase in G/C nucleotide frequencies. We show that this pattern, which covers a region tenfold larger than the conserved elements themselves, is an evolutionary consequence of a shift in the balance between gain and loss of G/C nucleotides and that it is correlated with nucleosome occupancy across multiple classes of epigenetic state. Evidence for compensatory evolution and analysis of SNP allele frequencies show that the evolutionary regime underlying this balance shift is likely to be non-neutral. These data suggest that current gaps in our understanding of genome function and evolutionary dynamics are explicable by a model of sparse sequence elements directly encoding for function, embedded into structural sequences that help to define the local and global epigenomic context of such functional elements.
MeSH term(s)	Animals ; Conserved Sequence/genetics ; Drosophila/genetics ; Evolution, Molecular ; Gene Frequency ; Genetic Drift ; Genome, Insect ; Polymorphism, Single Nucleotide ; Sequence Analysis, DNA ; Sequence Homology, Nucleic Acid
Language	English
Publishing date	2013-05-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1003512
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Article ; Online: ZFP281 drives a mesenchymal-like dormancy program in early disseminated breast cancer cells that prevents metastatic outgrowth in the lung.

Nobre, Ana Rita / Dalla, Erica / Yang, Jihong / Huang, Xin / Wullkopf, Lena / Risson, Emma / Razghandi, Pedram / Anton, Melisa Lopez / Zheng, Wei / Seoane, Jose A / Curtis, Christina / Kenigsberg, Ephraim / Wang, Jianlong / Aguirre-Ghiso, Julio A

Nature cancer

2022 Volume 3, Issue 10, Page(s) 1165–1180

Abstract: Increasing evidence shows that cancer cells can disseminate from early evolved primary lesions much earlier than the classical metastasis models predicted. Here, we reveal at a single-cell resolution that mesenchymal-like (M-like) and pluripotency-like ... ...

Abstract	Increasing evidence shows that cancer cells can disseminate from early evolved primary lesions much earlier than the classical metastasis models predicted. Here, we reveal at a single-cell resolution that mesenchymal-like (M-like) and pluripotency-like programs coordinate dissemination and a long-lived dormancy program of early disseminated cancer cells (DCCs). The transcription factor ZFP281 induces a permissive state for heterogeneous M-like transcriptional programs, which associate with a dormancy signature and phenotype in vivo. Downregulation of ZFP281 leads to a loss of an invasive, M-like dormancy phenotype and a switch to lung metastatic outgrowth. We also show that FGF2 and TWIST1 induce ZFP281 expression to induce the M-like state, which is linked to CDH1 downregulation and upregulation of CDH11. We found that ZFP281 not only controls the early dissemination of cancer cells but also locks early DCCs in a dormant state by preventing the acquisition of an epithelial-like proliferative program and consequent metastases outgrowth.
MeSH term(s)	Humans ; Fibroblast Growth Factor 2 ; Neoplasms ; Transcription Factors/genetics ; Lung
Chemical Substances	Fibroblast Growth Factor 2 (103107-01-3) ; Transcription Factors
Language	English
Publishing date	2022-09-01
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2662-1347
ISSN (online)	2662-1347
DOI	10.1038/s43018-022-00424-8
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Article ; Online: MARS-seq2.0: an experimental and analytical pipeline for indexed sorting combined with single-cell RNA sequencing.

Keren-Shaul, Hadas / Kenigsberg, Ephraim / Jaitin, Diego Adhemar / David, Eyal / Paul, Franziska / Tanay, Amos / Amit, Ido

Nature protocols

2019 Volume 14, Issue 6, Page(s) 1841–1862

Abstract: Human tissues comprise trillions of cells that populate a complex space of molecular phenotypes and functions and that vary in abundance by 4-9 orders of magnitude. Relying solely on unbiased sampling to characterize cellular niches becomes infeasible, ... ...

Abstract	Human tissues comprise trillions of cells that populate a complex space of molecular phenotypes and functions and that vary in abundance by 4-9 orders of magnitude. Relying solely on unbiased sampling to characterize cellular niches becomes infeasible, as the marginal utility of collecting more cells diminishes quickly. Furthermore, in many clinical samples, the relevant cell types are scarce and efficient processing is critical. We developed an integrated pipeline for index sorting and massively parallel single-cell RNA sequencing (MARS-seq2.0) that builds on our previously published MARS-seq approach. MARS-seq2.0 is based on >1 million cells sequenced with this pipeline and allows identification of unique cell types across different tissues and diseases, as well as unique model systems and organisms. Here, we present a detailed step-by-step procedure for applying the method. In the improved procedure, we combine sub-microliter reaction volumes, optimization of enzymatic mixtures and an enhanced analytical pipeline to substantially lower the cost, improve reproducibility and reduce well-to-well contamination. Data analysis combines multiple layers of quality assessment and error detection and correction, graphically presenting key statistics for library complexity, noise distribution and sequencing saturation. Importantly, our combined FACS and single-cell RNA sequencing (scRNA-seq) workflow enables intuitive approaches for depletion or enrichment of cell populations in a data-driven manner that is essential to efficient sampling of complex tissues. The experimental protocol, from cell sorting to a ready-to-sequence library, takes 2-3 d. Sequencing and processing the data through the analytical pipeline take another 1-2 d.
MeSH term(s)	Animals ; Cell Line ; Flow Cytometry/methods ; Gene Expression Profiling/methods ; Gene Library ; High-Throughput Nucleotide Sequencing/methods ; Humans ; Mice ; RNA/genetics ; Reproducibility of Results ; Single-Cell Analysis/methods ; Software ; Workflow
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2019-05-17
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2244966-8
ISSN	1750-2799 ; 1754-2189
ISSN (online)	1750-2799
ISSN	1754-2189
DOI	10.1038/s41596-019-0164-4
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Article ; Online: A myeloid-stromal niche and gp130 rescue in NOD2-driven Crohn's disease.

Nayar, Shikha / Morrison, Joshua K / Giri, Mamta / Gettler, Kyle / Chuang, Ling-Shiang / Walker, Laura A / Ko, Huaibin M / Kenigsberg, Ephraim / Kugathasan, Subra / Merad, Miriam / Chu, Jaime / Cho, Judy H

Nature

2021 Volume 593, Issue 7858, Page(s) 275–281

Abstract: Crohn's disease is a chronic inflammatory intestinal disease that is frequently accompanied by aberrant healing and stricturing complications. Crosstalk between activated myeloid and stromal cells is critical in the pathogenicity of Crohn's ... ...

Abstract	Crohn's disease is a chronic inflammatory intestinal disease that is frequently accompanied by aberrant healing and stricturing complications. Crosstalk between activated myeloid and stromal cells is critical in the pathogenicity of Crohn's disease
MeSH term(s)	Alleles ; Animals ; Collagen/metabolism ; Crohn Disease/metabolism ; Cytokine Receptor gp130/antagonists & inhibitors ; Cytokine Receptor gp130/metabolism ; Disease Models, Animal ; Female ; Fibroblasts/cytology ; Fibroblasts/metabolism ; Humans ; Ileitis/metabolism ; Indoles/pharmacology ; Interleukin-11/metabolism ; Lipopolysaccharide Receptors/metabolism ; Macrophages/cytology ; Macrophages/metabolism ; Male ; Myeloid Cells/cytology ; Myeloid Cells/metabolism ; Nod2 Signaling Adaptor Protein/metabolism ; Receptor, Platelet-Derived Growth Factor alpha/metabolism ; STAT3 Transcription Factor/metabolism ; Stromal Cells/cytology ; Stromal Cells/metabolism ; WT1 Proteins/metabolism ; Zebrafish ; Zebrafish Proteins/metabolism
Chemical Substances	Indoles ; Interleukin-11 ; Lipopolysaccharide Receptors ; NOD2 protein, human ; NOD2 protein, zebrafish ; Nod2 Signaling Adaptor Protein ; STAT3 Transcription Factor ; STAT3 protein, human ; WT1 Proteins ; Zebrafish Proteins ; Cytokine Receptor gp130 (133483-10-0) ; Collagen (9007-34-5) ; Receptor, Platelet-Derived Growth Factor alpha (EC 2.7.10.1) ; bazedoxifene (Q16TT9C5BK)
Language	English
Publishing date	2021-03-31
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-021-03484-5
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Article ; Online: The mutation spectrum in genomic late replication domains shapes mammalian GC content.

Kenigsberg, Ephraim / Yehuda, Yishai / Marjavaara, Lisette / Keszthelyi, Andrea / Chabes, Andrei / Tanay, Amos / Simon, Itamar

Nucleic acids research

2016 Volume 44, Issue 9, Page(s) 4222–4232

Abstract: Genome sequence compositions and epigenetic organizations are correlated extensively across multiple length scales. Replication dynamics, in particular, is highly correlated with GC content. We combine genome-wide time of replication (ToR) data, ... ...

Abstract	Genome sequence compositions and epigenetic organizations are correlated extensively across multiple length scales. Replication dynamics, in particular, is highly correlated with GC content. We combine genome-wide time of replication (ToR) data, topological domains maps and detailed functional epigenetic annotations to study the correlations between replication timing and GC content at multiple scales. We find that the decrease in genomic GC content at large scale late replicating regions can be explained by mutation bias favoring A/T nucleotide, without selection or biased gene conversion. Quantification of the free dNTP pool during the cell cycle is consistent with a mechanism involving replication-coupled mutation spectrum that favors AT nucleotides at late S-phase. We suggest that mammalian GC content composition is shaped by independent forces, globally modulating mutation bias and locally selecting on functional element. Deconvoluting these forces and analyzing them on their native scales is important for proper characterization of complex genomic correlations.
MeSH term(s)	Base Composition ; Cell Line, Tumor ; Chromatin/genetics ; DNA Replication ; Evolution, Molecular ; Genome, Human ; Humans ; Mutation
Chemical Substances	Chromatin
Language	English
Publishing date	2016-04-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkw268
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Article ; Online: Primate CpG islands are maintained by heterogeneous evolutionary regimes involving minimal selection.

Cohen, Netta Mendelson / Kenigsberg, Ephraim / Tanay, Amos

Cell

2011 Volume 145, Issue 5, Page(s) 773–786

Abstract: Mammalian CpG islands are key epigenomic elements that were first characterized experimentally as genomic fractions with low levels of DNA methylation. Currently, CpG islands are defined based on their genomic sequences alone. Here, we develop ... ...

Abstract	Mammalian CpG islands are key epigenomic elements that were first characterized experimentally as genomic fractions with low levels of DNA methylation. Currently, CpG islands are defined based on their genomic sequences alone. Here, we develop evolutionary models to show that several distinct evolutionary processes generate and maintain CpG islands. One central evolutionary regime resulting in enriched CpG content is driven by low levels of DNA methylation and consequentially low rates of CpG deamination. Another major force forming CpG islands is biased gene conversion that stabilizes constitutively methylated CpG islands by balancing rapid deamination with CpG fixation. Importantly, evolutionary analysis and population genetics data suggest that selection for high CpG content is not a significant factor contributing to conservation of CpGs in differentially methylated regions. The heterogeneous, but not selective, origins of CpG islands have direct implications for the understanding of DNA methylation patterns in healthy and diseased cells.
MeSH term(s)	Animals ; CpG Islands ; DNA Methylation ; Deamination ; Evolution, Molecular ; Gene Conversion ; Humans ; Mammals/genetics ; Mice ; Models, Genetic ; Phylogeny
Language	English
Publishing date	2011-05-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2011.04.024
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Article ; Online: Widespread compensatory evolution conserves DNA-encoded nucleosome organization in yeast.

Kenigsberg, Ephraim / Bar, Amir / Segal, Eran / Tanay, Amos

PLoS computational biology

2010 Volume 6, Issue 12, Page(s) e1001039

Abstract: Evolution maintains organismal fitness by preserving genomic information. This is widely assumed to involve conservation of specific genomic loci among species. Many genomic encodings are now recognized to integrate small contributions from multiple ... ...

Abstract	Evolution maintains organismal fitness by preserving genomic information. This is widely assumed to involve conservation of specific genomic loci among species. Many genomic encodings are now recognized to integrate small contributions from multiple genomic positions into quantitative dispersed codes, but the evolutionary dynamics of such codes are still poorly understood. Here we show that in yeast, sequences that quantitatively affect nucleosome occupancy evolve under compensatory dynamics that maintain heterogeneous levels of A+T content through spatially coupled A/T-losing and A/T-gaining substitutions. Evolutionary modeling combined with data on yeast polymorphisms supports the idea that these substitution dynamics are a consequence of weak selection. This shows that compensatory evolution, so far believed to affect specific groups of epistatically linked loci like paired RNA bases, is a widespread phenomenon in the yeast genome, affecting the majority of intergenic sequences in it. The model thus derived suggests that compensation is inevitable when evolution conserves quantitative and dispersed genomic functions.
MeSH term(s)	Base Composition/genetics ; Computational Biology ; DNA, Fungal/genetics ; Evolution, Molecular ; Gene Frequency ; Models, Genetic ; Mutation ; Nucleosomes/genetics ; Polymorphism, Single Nucleotide ; Saccharomyces cerevisiae/genetics ; Sequence Alignment ; Sequence Analysis, DNA
Chemical Substances	DNA, Fungal ; Nucleosomes
Language	English
Publishing date	2010-12-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1001039
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Article: Peripheral Transcriptomics in Acute and Long-Term Kidney Dysfunction in SARS-CoV2 Infection.

Jayaraman, Pushkala / Rajagopal, Madhumitha / Paranjpe, Ishan / Liharska, Lora / Suarez-Farinas, Mayte / Thompson, Ryan / Del Valle, Diane Marie / Beckmann, Noam / Oh, Wonsuk / Gulamali, Faris F / Kauffman, Justin / Gonzalez-Kozlova, Edgar / Dellepiane, Sergio / Vasquez-Rios, George / Vaid, Akhil / Jiang, Joy / Chen, Annie / Sakhuja, Ankit / Chen, Steven /

Kenigsberg, Ephraim / He, John Cijiang / Coca, Steven G / Chan, Lili / Schadt, Eric / Merad, Miram / Kim-Schulze, Seunghee / Gnjatic, Sacha / Tsalik, Ephraim / Langley, Raymond / Charney, Alexander W / Nadkarni, Girish N

medRxiv : the preprint server for health sciences

2023

Abstract: Background: Acute kidney injury (AKI) is common in hospitalized patients with SARS-CoV2 infection despite vaccination and leads to long-term kidney dysfunction. However, peripheral blood molecular signatures in AKI from COVID-19 and their association ... ...

Abstract	Background: Acute kidney injury (AKI) is common in hospitalized patients with SARS-CoV2 infection despite vaccination and leads to long-term kidney dysfunction. However, peripheral blood molecular signatures in AKI from COVID-19 and their association with long-term kidney dysfunction are yet unexplored. Methods: In patients hospitalized with SARS-CoV2, we performed bulk RNA sequencing using peripheral blood mononuclear cells(PBMCs). We applied linear models accounting for technical and biological variability on RNA-Seq data accounting for false discovery rate (FDR) and compared functional enrichment and pathway results to a historical sepsis-AKI cohort. Finally, we evaluated the association of these signatures with long-term trends in kidney function. Results: Of 283 patients, 106 had AKI. After adjustment for sex, age, mechanical ventilation, and chronic kidney disease (CKD), we identified 2635 significant differential gene expressions at FDR<0.05. Top canonical pathways were Conclusions: We show that AKI in SARS-CoV2 is a multifactorial process with mitochondrial dysfunction driven by ER stress whereas long-term kidney function decline is associated with cardiac structure and function and immune dysregulation. Functional overlap with sepsis-AKI also highlights common signatures, indicating generalizability in therapeutic approaches. Significance statement: Peripheral transcriptomic findings in acute and long-term kidney dysfunction after hospitalization for SARS-CoV2 infection are unclear. We evaluated peripheral blood molecular signatures in AKI from COVID-19 (COVID-AKI) and their association with long-term kidney dysfunction using the largest hospitalized cohort with transcriptomic data. Analysis of 283 hospitalized patients of whom 37% had AKI, highlighted the contribution of mitochondrial dysfunction driven by endoplasmic reticulum stress in the acute stages. Subsequently, long-term kidney function decline exhibits significant associations with markers of cardiac structure and function and immune mediated dysregulation. There were similar biomolecular signatures in other inflammatory states, such as sepsis. This enhances the potential for repurposing and generalizability in therapeutic approaches.
Language	English
Publishing date	2023-10-27
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.25.23297469
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Article ; Online: TREM2 macrophages drive NK cell paucity and dysfunction in lung cancer.

Park, Matthew D / Reyes-Torres, Ivan / LeBerichel, Jessica / Hamon, Pauline / LaMarche, Nelson M / Hegde, Samarth / Belabed, Meriem / Troncoso, Leanna / Grout, John A / Magen, Assaf / Humblin, Etienne / Nair, Achuth / Molgora, Martina / Hou, Jinchao / Newman, Jenna H / Farkas, Adam M / Leader, Andrew M / Dawson, Travis / D'Souza, Darwin /

Hamel, Steven / Sanchez-Paulete, Alfonso Rodriguez / Maier, Barbara / Bhardwaj, Nina / Martin, Jerome C / Kamphorst, Alice O / Kenigsberg, Ephraim / Casanova-Acebes, Maria / Horowitz, Amir / Brown, Brian D / De Andrade, Lucas Ferrari / Colonna, Marco / Marron, Thomas U / Merad, Miriam

Nature immunology

2023 Volume 24, Issue 5, Page(s) 792–801

Abstract: Natural killer (NK) cells are commonly reduced in human tumors, enabling many to evade surveillance. Here, we sought to identify cues that alter NK cell activity in tumors. We found that, in human lung cancer, the presence of NK cells inversely ... ...

Abstract	Natural killer (NK) cells are commonly reduced in human tumors, enabling many to evade surveillance. Here, we sought to identify cues that alter NK cell activity in tumors. We found that, in human lung cancer, the presence of NK cells inversely correlated with that of monocyte-derived macrophages (mo-macs). In a murine model of lung adenocarcinoma, we show that engulfment of tumor debris by mo-macs triggers a pro-tumorigenic program governed by triggering receptor expressed on myeloid cells 2 (TREM2). Genetic deletion of Trem2 rescued NK cell accumulation and enabled an NK cell-mediated regression of lung tumors. TREM2
MeSH term(s)	Humans ; Mice ; Animals ; Killer Cells, Natural ; Macrophages ; Lung Neoplasms ; Myeloid Cells ; Membrane Glycoproteins/genetics ; Receptors, Immunologic/genetics
Chemical Substances	TREM2 protein, human ; Membrane Glycoproteins ; Receptors, Immunologic ; Trem2 protein, mouse
Language	English
Publishing date	2023-04-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-023-01475-4
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