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Georgiou, G.

Publications and source records attributed to Georgiou, G..

At least 19 recordsLinked to original sources

Serum IgM crosslinks hepatitis B subviral particles into supramolecular immune complexes

Hepatitis B virus (HBV)-infected cells release hepatitis B surface antigen (HBsAg)-rich subviral particles (SVPs) in large excess over infectious virions. SVPs bind antibodies against HBsAg (anti-HBs), including neutralizing antibodies, but the physical products of antibody capture in human blood are uncharacterized. Here we used cryo-electron tomography (cryo-ET) to image HBsAg-enriched serum from a patient with severe acute Hepatitis B and observed three-dimensional assemblies of intact IgM-SVP immune complexes. These associations persisted at a lower particle density and were validated by a spatial-randomization null model. Subtomogram averaging and single-particle cryo-electron microscopy (cryo-EM) identified three serum IgM Fc-core assemblies, IgM-J-CD5L, IgM-J and IgM-J-SC, with cryo-EM maps reaching 2.8 angstrom resolution. Mapping these Fc core assemblies into tomograms revealed full-length IgM engaging individual SVPs through several Fab arms and bridging neighboring particles into immune complex networks containing multiple IgM molecules and SVPs. Thus, serum IgM uses multivalent Fab interactions to crosslink HBsAg-rich SVPs into supramolecular immune complexes. This observation extends the SVP decoy model from passive antibody sequestration to higher-order particle organization.

molecular biology↗

Antibodies with Engineered Fc Domains Having Absolute Binding Selectivity to either FcγRIIa or FcγRI Delineate the Respective Effector Phenotypes by Human Monocytes and Macrophages

IgG1 immune complexes bind to all the Fc{gamma} receptors (Fc{gamma}R) expressed on myeloid cells, making it challenging to determine the precise role of each Fc{gamma}R on Fc effector phenotypes. Here we report the engineering of Fc2KG, an aglycosylated human IgG1 Fc domain that binds with near physiological affinity to Fc{gamma}RIIa/b with no detectable binding to any other Fc{gamma}Rs. Crystallographic analysis elucidated the structural basis of how mutations in the Fc domain compensate for the absence of the N297 glycan and enable selective binding. Using single-cell phagocytosis assays, we show that particles opsonized with Fc-engineered antibodies formatted with Fc2KG or with an Fc domain that binds only Fc{gamma}RI (Fc5), are ingested by THP-1 cells with near identical kinetics. We find that with CD16+ primary human monocytes, selective Fc{gamma}RII engagement is a major contributor to the ADCP mediated by wild-type IgG1. Additionally, we showed that Fc2KG formatted antibodies induce high levels of GM-CSF. With M1-like monocyte-derived human macrophages, trastuzumab formatted with wild-type IgG1 Fc, with Fc2KG or Fc5 were all equally proficient in the trogocytotic killing of opsonized SK-BR-3 HER2+ cells but only Fc{gamma}RI engagement led to secretion of proinflammatory cytokines. Collectively, our results highlight how precisely tuned, Fc-engineered antibodies can be deployed to answer long-standing questions regarding the precise effector functions mediated by human Fc{gamma}Rs, information which is key for the optimization of therapeutic antibodies.

immunology↗

Epstein-Barr virus transformation creates a methionine-dependent ferroptosis vulnerability in B cells

Epstein-Barr virus (EBV) causes over 200,000 cancers annually, including immunoblastic lymphomas in immunosuppressed hosts. Most transformed cells arrest, yet survive when deprived of the essential amino acid methionine. We instead find that EBV transformed lymphoblastoid cell lines (LCLs), which model the EBV latency III program-driven B-cell lymphoproliferative diseases of immunosuppressed hosts, rapidly die upon methionine restriction. Methionine restriction elevated LCL lipid reactive oxygen species and triggered ferroptosis. Whereas methionine restriction hypomethylates the EBV genome and triggers viral reactivation in latency I Burkitt cells by lowering the cellular methylation potential, the LCL latency III program instead redirected methionine toward redox defense, without altering the SAM/SAH ratio. Stable-isotope tracing revealed that latency III strongly induces transsulfuration, synthesizing cysteine de novo to support glutathione pools. The EBV oncoprotein LMP2A, which mimics B-cell receptor signaling, supported newly infected human B cell cystathionine-{beta}-synthase and cystathionine-{gamma}-lyase expression and methionine dependence, phenocopied by immunoglobulin crosslinking. In vivo, dietary methionine restriction impaired LCL xenograft outgrowth and depleted tumor cystine. Combined methioninase and cyst(e)inase administration blocked both cysteine sources, collapsed tumor glutathione levels, and triggered ferroptosis. Our results define methionine metabolism as a targetable ferroptosis vulnerability of EBV-transformed B cells. HighlightsO_LIMethionine restriction triggers EBV-transformed lymphoblastoid B cell ferroptosis C_LIO_LIEBV latency III induces transsulfuration to sustain LCL cysteine and glutathione C_LIO_LIMethioninase or dietary methionine restriction strongly impair LCL growth in vivo C_LIO_LIMethioninase plus cyst(e)inase collapses xenograft GSH levels and drives ferroptosis C_LI

biochemistry↗

Broad Sarbecovirus Neutralization by an S2-Directed Plasma Antibody Defines a New Site of Vulnerability in SARS-like Viruses

The repeated emergence of pathogenic coronaviruses highlights the continual threat of zoonotic spillover events and the need to understand conserved regions of the viral spike protein that influence immune recognition. Here, we employ high-resolution proteomic analysis of circulating immunoglobulins to characterize the antibody response to the SARS-CoV-2 spike protein in vaccinated and infected individuals. We recombinantly expressed abundant plasma IgG lineages and identified nine antibodies targeting the highly conserved S2 spike subunit. Most of these S2-reactive plasma mAbs (7 of 9) exhibited neutralizing activity against pangolin coronavirus, while one mAb (SC45) demonstrated potent (IC50 < 1 {micro}g/mL) neutralizing activity against both pangolin and bat sarbecoviruses RsSHC014 and WIV1. Additionally, SC45 exhibited potent prophylactic efficacy in the K18-hACE2 mouse model challenged with Pangolin-Guangdong CoV MP789 (Pg-CoV), significantly reducing lung viral replication at day 4 post-infection. The cryo-EM structure of SC45 bound to the prefusion-stabilized S2 domain of Pg-CoV reveals that SC45 targets a novel, conserved epitope in the connector domain. Strikingly, even though SC45 was the most abundant antibody ([~]13%) of anti-spike plasma IgG in an infected patient and binds to both SARS-CoV-2 and Pg-CoV spike with comparable affinities, it fails to neutralize early (D614G and Omicron BA.1) SARS-CoV-2 variants. Together, these findings identify a conserved site of vulnerability in the spike S2 subunit which informs on potential mechanisms of antibody immunity to zoonotic coronaviruses.

immunology↗

Structure-Function Analysis of the FCRL5-IgG1 Fc Complex Reveals an Unappreciated Effect of Fc-Silent Antibodies on B cells

Human Fc receptor-like 5 (FCRL5) is a low-affinity IgG Fc receptor expressed on various B cell subsets and a potential therapeutic target. We discovered that commonly used Fc-silencing mutations, designed to prevent interactions between the Fc{gamma} receptors on immune cells and the Fc domain of therapeutic IgG, do not prevent binding to FCRL5. As a result, unintended interactions between Fc-silent therapeutic IgG and human B cells may occur. We isolated a well-expressed variant of the Fc-binding portion of human FCRL5 by directed evolution and used structural modeling to guide the engineering of a human IgG1 Fc variant with approximately 100-fold higher affinity for FCRL5, enabling us to produce FCRL5:Fc complexes in solution. Native mass spectrometry, size exclusion chromatography, and the crystal structure of the FCRL5- IgG1 Fc complex solved at 3.4 [A] indicate that the two proteins bind in a 1:1 stoichiometry. Furthermore, the structure revealed that FCRL5 binds to IgG1 Fc in a manner completely distinct from that of previously characterized Fc-binding proteins, such as Fc{gamma} receptors, explaining why most Fc-silencing mutations do not disrupt FCRL5 binding. We demonstrate that selective cross-linking of FCRL5 with the B cell receptor (BCR) in cis, using Fc-engineered antibodies with either physiological or enhanced FCRL5 affinity, inhibits Ca2+ flux in FCRL5-expressing B cells. We compare this effect with the selective co-ligation of Fc{gamma}RIIb with the BCR. Our work demonstrates that FCRL5 interacts with human IgG Fc in a distinctive manner and that engagement of FCRL5 by Fc-silent therapeutic IgG could influence B cell function.

bioengineering↗

Synergistic non-neutralizing plasma antibodies to PfRH5 drive potent malaria parasite growth inhibition

An effective blood-stage vaccine is needed to protect against malaria pre-erythrocytic stage breakthrough. P. falciparum reticulocyte-binding protein homolog 5 (PfRH5) has emerged as a promising blood-stage vaccine antigen candidate, reducing parasite growth in humans during malaria challenge and showing field efficacy in children. Here, we characterize the human plasma IgG response to the RH5.1 vaccine candidate at monoclonal resolution, revealing that plasma repertoires are dominated by abundant, non-neutralizing antibodies. Using oligoclonal reconstitution experiments, in which defined pools of recombinant plasma mAbs are reassembled and functionally tested, we map how individual antibody interactions shape parasite growth inhibition activity. This approach allows us to discern which antibodies, within a polyclonal setting, act additively or synergistically, thereby revealing the emergent properties of anti-PfRH5 IgG. We further show that IgG lineages targeting linear epitopes lack neutralizing activity, while non-neutralizing IgG lineages that bind conformational epitopes can exhibit potent, interdependent synergy with each other and with neutralizing mAbs. These synergistic antibodies were identified in the plasma IgG compartments of five volunteers and highlight non-neutralizing PfRH5 epitopes that are critical for polyclonal-mediated growth inhibition. Our findings have broad implications for PfRH5 vaccine immunogen engineering and the role of non-neutralizing antibodies in infectious disease immunity.

immunology↗

Imprinted antibody lineages can persist for half a century and dominate cross-neutralizing recall responses to poliovirus

Humoral immunity depends on a dynamic interplay between circulating polyclonal IgG antibodies and long-lived memory B cells (MBC). To elucidate this relationship, we integrated B-cell receptor sequencing with plasma IgG immunoproteomics to identify and quantify the recall response (plasma IgG and MBC) to inactivated poliovirus vaccine (IPV) in eight adults, 24-55 years after their childhood immunization. IPV immunization elicited highly skewed plasma IgG recall repertoires, dominated by a small subset ([~]8%) of total antibody lineages that were detectable prior to boosting (i.e., "pre-existing"). These IgG lineages spiked logarithmically in abundance ([~]102-104 fold-increase) and potently cross-neutralized multiple PV serotypes in vitro (titers [&ge;] 1:105). Notably, these dominant plasma IgG lineages were clonally linked to class-switched MBCs that circulated in blood 21 days post-boost and bore heavily mutated VH and VL variable region genes. Importantly, IPV-primed ex vivo B-cell cultures (MIMIC, Modular IMmune In vitro Construct) yielded clonal expansions that mirrored the dominant post-boost plasma IgG lineages in vivo, providing an in vitro mechanistic correlate of recall immunity. Together these findings demonstrate a decades-long interconnectivity between persistent MBC clones and the serological IgG repertoire. They further highlight the central role of immunological imprinting, whereby cross-reactive MBC clones--originally primed in childhood--can be reactivated to dominate the circulating IgG recall response more than 50 years after initial exposure.

immunology↗

Selective decoupling of IgG1 binding to viral Fc receptorsrestores antibody-mediated NK cell activation against HCMV-infected cells

A key mechanism of antiviral antibodies is to bind cell-surface viral antigens and activate cellular immunity to clear infected cells, yet antibodies targeting human cytomegalovirus (HCMV) have exhibited limited efficacy. This appears due to HCMVs multiple immune evasion mechanisms, including viral receptors (vFc{gamma}Rs) which bind human IgG Fc domains to co-operatively inhibit Fc activation of host Fc{gamma} receptors and impair Fc-mediated effector functions. We biochemically characterized and evaluated the functions of two highly conserved vFc{gamma}Rs, gp34 and gp68, and mapped their binding epitopes on the Fc domain. Based on this information, we then engineered Fc variants that retain binding to CD16A, which is essential for NK activation, and to FcRn but have markedly attenuated binding to gp34 and gp68. IgG1 antibodies targeting the gB fusogen with engineered Fc domains were not internalized by infected cells, mediated enhanced CD16A activation and limited viral spread in HCMV-infected fibroblasts more effectively than wild-type Fc. Together, this work demonstrates a strategy to enhance the efficacy of antibody therapies to clear HCMV infections. HighlightsO_LIHost and HCMV FcR compete for IgG1 binding but engage different residues. C_LIO_LIFc-engineering abrogates viral FcR antagonism while retaining CD16A activation. C_LIO_LIAntibodies that resist vFcR capture promote superior ADCC against infected cells. C_LIO_LIDesigner Fc domains complement Fabs to create enhanced disease-specific therapies. C_LI

immunology↗

Stage-specific gene ratios highlight genes and mechanisms related to presymptomatic and symptomatic Multiple Myeloma

Background/aimMultiple Myeloma is the second most common blood cancer, characterised by the accumulation of malignant plasma cells and the production of large amounts of a monoclonal immunoglobulin protein, in the bone marrow. The identification and progression/behaviour of molecular markers across stages remains a scientific challenge. This work aims to provide a holistic approach to the understanding of the disease progression, providing specific methodologies and candidate biomarkers, able to characterise and distinguish the disease state across stages. Materials and methodsTwo large bulk RNA datasets were used to collect and integrate stage-specific information at the gene level by means of: (a) differential expression analysis to obtain differential expressed genes (DEGs), (b) a recently introduced computational methodology able to detect monotonically expressed genes (MEGs), (c) a proposed computational methodology that uses pairs of MEGs at sample level, to classify and discriminate different stages of Multiple Myeloma. Additional numerical metrics were applied to rank the performance of these pairs across samples, facilitating the characterization and differentiation of disease stages. Validation was conducted using five additional external datasets, which were then utilised to enrich the final selection of top-rated genes identified from the two bulk RNA datasets under study. The final top-ranked genes were further used for pathway enrichment analysis in order to provide candidate pathways per stage. ResultsWe first show that MEGs provide better statistics than DEGs, both at gene and pathway level analysis. Secondly, we show that the proposed computational methodology by means of MEGs reveals short lists of high discriminative genes across stages, which in turn highlight significant groups of pathways. ConclusionWe integrated traditional analysis of DEGs with a recently introduced methodology for identifying MEGs, creating a novel computational approach capable of identifying highly discriminative genes and pathways that can serve as candidate markers for stage identification in a single sample. HighlightsO_LIA novel computational approach was used to identify Monotonically Expressed Genes (MEGs) whose expression was constantly increasing or decreasing. Genes such as RB1, CD27, TP53, and MCL1, previously highlighted in Multiple Myeloma, showed a consistent monotonic pattern, providing potential indicators for tracking the progression from the pre-malignant stages to active Multiple Myeloma. C_LIO_LIThe study calculated gene pair ratios using MEGs characterised by normal distribution and low dispersion. These ratios effectively distinguished healthy from disease samples, although the discrimination between disease stages (MGUS, SMM, MM) was less clear due to their overlapping molecular profiles. C_LIO_LIEnrichment analysis of significant gene pairs identified critical pathways affected during Multiple Myeloma progression, such as bone disease-related calcium pathways, glucocorticoid-regulated functions, and cardiac and neurological systems. These findings align with known clinical manifestations in MM patients, such as bone disease and amyloid cardiomyopathy. C_LIO_LIThe gene lists generated from our computational approach were validated against internal and external datasets, confirming their applicability. The methodology showed promise in identifying candidate genes for disease progression and could be applied to other diseases to uncover novel gene pairs not highlighted by traditional analyses. C_LI

bioinformatics↗

Repertoire, function, and structure of serological antibodies induced by the R21/Matrix-M malaria vaccine

The World Health Organization recently recommended the programmatic use of R21/Matrix-M vaccine for Plasmodium falciparum malaria prevention in children living in malaria-endemic areas. To determine its effects on humoral immunity, we conducted a proteomic analysis of polyclonal IgG antibodies directed against the NANP tetrapeptide of the circumsporozoite protein (CSP) which comprises the vaccines core immunogen. In ten malaria-naive adult volunteers, R21/Matrix-M induced polarized IgG anti-NANP repertoires, heavily skewed for IGHV3-30/3-33 genes bearing minimal somatic mutation, which remained static in composition following a controlled human malaria infection challenge. Notably, these vaccine-generated antibodies cross-reacted with another protective CSP epitope, the N-terminal junction region, despite its absence from the R21 construct. NANP-specific IGHV3-30/3-33 monoclonal antibodies mined from polyclonal IgG repertoires blocked sporozoite invasion in vitro and prevented parasitemia in vivo. Overall, R21/Matrix-M elicits polarized, minimally mutated, polyclonal IgG responses that can target multiple protective CSP epitopes, offering molecular insight into the serological basis for its demonstrated efficacy against P. falciparum malaria.

immunology↗

Mutability and hypermutation antagonize immunoglobulin codon optimality

The efficacy of polyclonal antibody responses is inherently linked to paratope diversity, as generated through V(D)J recombination and somatic hypermutation (SHM). These processes arose in early jawed vertebrates; however, little is known about how immunoglobulin diversity, mutability, and hypermutation have evolved in tandem with another more ubiquitous feature of protein-coding DNA - codon optimality. Here, we explore these relationships through analysis of germline IG genes, natural V(D)J repertoires, serum VH usage, and monoclonal antibody (mAb) expression, each through the lens of multiple optimality metrics. Strikingly, proteomic serum IgG sequencing showed that germline IGHV codon optimality positively correlated with VH representation after influenza vaccination, and in vitro, codon deoptimization of mAbs with synonymous amino acid sequences caused consistent expression loss. Germline V genes exhibit a range of codon optimality that is maintained by functionality, and inversely related to mutability. SHM caused a load-dependent deoptimization of IGH VDJ repertoires within human tonsils, bone marrow, and lymph nodes (including SARS-CoV-2-specific clones from mRNA vaccinees), influenza-infected mice, and zebrafish. Comparison of natural mutation profiles to true random suggests the presence of selective pressures that constrain deoptimization. These findings shed light on immunoglobulin evolution, providing unanticipated insights into the antagonistic relationship between variable region diversification, codon optimality, and antibody secretion; ultimately, the need for diversity takes precedence over that for the most efficient expression of the antibody repertoire.

immunology↗

Hybrid immunity to SARS-CoV-2 arises from serological recall of IgG antibodies distinctly imprinted by infection or vaccination

We used plasma IgG proteomics to study the molecular composition and temporal durability of polyclonal IgG antibodies triggered by ancestral SARS-CoV-2 infection, vaccination, or their combination ("hybrid immunity"). Infection, whether primary or post-vaccination, mainly triggered an anti-spike antibody response to the S2 domain, while vaccination predominantly induced anti-RBD antibodies. Immunological imprinting persisted after a secondary (hybrid) exposure, with >60% of the ensuing serological response originating from the initial antibodies generated during the first exposure. We highlight one instance where hybrid immunity arising from breakthrough infection resulted in a marked increase in the breadth and affinity of a highly abundant vaccination-elicited plasma IgG antibody, SC27. With an intrinsic binding affinity surpassing a theoretical maximum (KD < 5 pM), SC27 demonstrated potent neutralization of various SARS-CoV-2 variants and SARS-like zoonotic viruses (IC50 [~]0.1-1.75 nM) and provided robust protection in vivo. Cryo-EM structural analysis unveiled that SC27 binds to the RBD class 1/4 epitope, with both VH and VL significantly contributing to the binding interface. These findings suggest that exceptionally broad and potent antibodies can be prevalent in plasma and can largely dictate the nature of serological neutralization. HIGHLIGHTS{blacksquare} Infection and vaccination elicit unique IgG antibody profiles at the molecular level {blacksquare}Immunological imprinting varies between infection (S2/NTD) and vaccination (RBD) {blacksquare}Hybrid immunity maintains the imprint of first infection or first vaccination {blacksquare}Hybrid immune IgG plasma mAbs have superior neutralization potency and breadth

immunology↗

Infant antibody repertoires during the first two years of influenza vaccination

The first encounter with influenza virus biases later immune responses. This "immune imprinting", formerly from infection within a few years of birth, is in the U.S. now largely from immunization with a quadrivalent, split vaccine (IIV4). In a pilot study of IIV4 imprinting, we characterized, by single-B-cell cultures, NextGen sequencing, and plasma antibody proteomics, the primary antibody responses to influenza in two infants during their first two years of seasonal influenza vaccination. One infant, who received only a single vaccination in Year 1, contracted an influenza B (IBV) infection between the two years, allowing us to compare imprinting by infection and vaccination. That infant had a shift in hemagglutinin (HA)-reactive B-cell specificity from largely influenza A (IAV)-specific in Year 1 to IBV-specific in Year 2, both before and after vaccination. HA-reactive B cells from the other infant maintained a more evenly distributed specificity. In Year 2, class-switched HA-specific B cell IGHV somatic hypermutation (SHM) levels reached average levels seen in adults. The HA-reactive plasma antibody repertoires of both infants comprised a relatively small number of antibody clonotypes, with one or two very abundant clonotypes. Thus, after the Year 2 boost, both infants had overall B cell profiles that resembled those of adult controls. ImportanceInfluenza virus is a moving target for the immune system. Variants emerge that escape protection from antibodies elicited by a previously circulating variant ("antigenic drift"). The immune system usually responds to a drifted influenza virus by mutating existing antibodies rather than by producting entirely new ones. Thus, immune memory of the earliest influenza exposure has a major influence on later responses to infection or vaccination ("immune imprinting"). In the many studies of influenza immunity in adult subjects, imprinting has been from an early infection, since only in the past two decades have infants received influenza immunizations. The work reported in this paper is a pilot study of imprinting in two infants by the flu vaccine, which they received before experiencing an influenza infection. The results suggest that a quadrivalent (four-subtype) vaccine may provide an immune imprint less dominated by one subtype than does a monovalent infection.

immunology↗

Synthetic repertoires derived from convalescent COVID-19 patients enable discovery of SARS-CoV-2 neutralizing antibodies and a novel quaternary binding modality

The ongoing evolution of SARS-CoV-2 into more easily transmissible and infectious variants has sparked concern over the continued effectiveness of existing therapeutic antibodies and vaccines. Hence, together with increased genomic surveillance, methods to rapidly develop and assess effective interventions are critically needed. Here we report the discovery of SARS-CoV-2 neutralizing antibodies isolated from COVID-19 patients using a high-throughput platform. Antibodies were identified from unpaired donor B-cell and serum repertoires using yeast surface display, proteomics, and public light chain screening. Cryo-EM and functional characterization of the antibodies identified N3-1, an antibody that binds avidly (Kd,app = 68 pM) to the receptor binding domain (RBD) of the spike protein and robustly neutralizes the virus in vitro. This antibody likely binds all three RBDs of the trimeric spike protein with a single IgG. Importantly, N3-1 equivalently binds spike proteins from emerging SARS-CoV-2 variants of concern, neutralizes UK variant B.1.1.7, and binds SARS-CoV spike with nanomolar affinity. Taken together, the strategies described herein will prove broadly applicable in interrogating adaptive immunity and developing rapid response biological countermeasures to emerging pathogens.

synthetic biology↗

A prevalent focused human antibody response to the influenza hemagglutinin head interface

Novel animal influenza viruses emerge, initiate pandemics and become endemic seasonal variants that have evolved to escape from prevalent herd immunity. These processes often outpace vaccine-elicited protection. Focusing immune responses on conserved epitopes may impart durable immunity. We describe a focused, protective antibody response, abundant in memory and serum repertoires, to a conserved region at the influenza hemagglutinin head interface. Structures of eleven examples, eight reported here, from seven human donors demonstrate the convergence of responses on a single epitope. The eleven are genetically diverse, with one class having a common, IG{kappa}V1-39, light chain. All of the antibodies bind HAs from multiple serotypes. The lack of apparent genetic restriction and potential for elicitation by more than one serotype may explain their abundance. We define the head interface as a major target of broadly protective antibodies with the potential to influence the outcomes of influenza infection.

immunology↗

Prevalent, protective, and convergent IgG recognition of SARS-CoV-2 non-RBD spike epitopes in COVID-19 convalescent plasma

Although humoral immunity is essential for control of SARS-CoV-2, the molecular composition, binding epitopes and effector functions of the immunoglobulin G (IgG) antibodies that circulate in blood plasma following infection are unknown. Proteomic deconvolution of the circulating IgG repertoire (Ig-Seq1) to the spike ectodomain (S-ECD2) in four convalescent study subjects revealed that the plasma response is oligoclonal and directed predominantly (>80%) to S-ECD epitopes that lie outside the receptor binding domain (RBD). When comparing antibodies directed to either the RBD, the N-terminal domain (NTD) or the S2 subunit (S2) in one subject, just four IgG lineages (1 anti-S2, 2 anti-NTD and 1 anti-RBD) accounted for 93.5% of the repertoire. Although the anti-RBD and one of the anti-NTD antibodies were equally potently neutralizing in vitro, we nonetheless found that the anti-NTD antibody was sufficient for protection to lethal viral challenge, either alone or in combination as a cocktail where it dominated the effect of the other plasma antibodies. We identified in vivo protective plasma anti-NTD antibodies in 3/4 subjects analyzed and discovered a shared class of antibodies targeting the NTD that utilize unmutated or near-germline IGHV1-24, the most electronegative IGHV gene in the human genome. Structural analysis revealed that binding to NTD is dominated by interactions with the heavy chain, accounting for 89% of the entire interfacial area, with germline residues uniquely encoded by IGHV1-24 contributing 20% (149 [A]2). Together with recent reports of germline IGHV1-24 antibodies isolated by B-cell cloning3,4 our data reveal a class of shared IgG antibodies that are readily observed in convalescent plasma and underscore the role of NTD-directed antibodies in protection against SARS-CoV-2 infection.

immunology↗

ANANSE: An enhancer network-based computational approach for predicting key transcription factors in cell fate determination

Proper cell fate determination is largely orchestrated by complex gene regulatory networks centered around transcription factors. However, experimental elucidation of key transcription factors that drive cellular identity is currently often intractable. Here, we present ANANSE (ANalysis Algorithm for Networks Specified by Enhancers), a network-based method that exploits enhancer-encoded regulatory information to identify the key transcription factors in cell fate determination. As cell type-specific transcription factors predominantly bind to enhancers, we use regulatory networks based on enhancer properties to prioritize transcription factors. First, we predict genome-wide binding profiles of transcription factors in various cell types using enhancer activity and transcription factor binding motifs. Subsequently, applying these inferred binding profiles, we construct cell type-specific gene regulatory networks, and then predict key transcription factors controlling cell fate transitions using differential networks between cell types. This method outperforms existing approaches in correctly predicting major transcription factors previously identified to be sufficient for trans-differentiation. Finally, we apply ANANSE to define an atlas of key transcription factors in 18 normal human tissues. In conclusion, we present a ready-to-implement computational tool for efficient prediction of transcription factors in cell fate determination and to study transcription factor-mediated regulatory mechanisms. ANANSE is freely available at https://github.com/vanheeringen-lab/ANANSE.

systems biology↗

Comprehensive and Integrated Genomic Characterization of Human Immunome in Cancer

Genetic alterations in immune-related pathways are common hallmarks of cancer. However, to realize the full potential of immunotherapy, a comprehensive understanding of immune networks and how mutations impact network structure and functional output across cancer types is instrumental. Herein we systematically interrogated somatic mutations that could express neoantigens and alter immune responses in cancer patients compared to wild-type controls. To do so, we developed a network-based immunogenomics model (NIPPER) with scoring systems to prioritize critical genes and mutations eliciting differential HLA binding affinity and alternate responses to immunotherapy. These mutations are enriched in essential protein domains and often alter tumor infiltration by immune cells, affecting T cell receptor repertoire and B cell clonal expansion. Furthermore, we devised an interactome network propagation framework integrated with drug associated gene signatures to identify potential immunomodulatory drug candidates. Together, our systems-level analysis results help interpret the heterogeneous immune responses among patients, and serve as a resource for future functional studies and targeted therapeutics. SignificanceCancer cells induce specific immune-related pathway perturbations by mutations, transcriptional dysregulation, and integration of multi-omics data can help identify critical molecular determinants for effective targeted therapeutics.

immunology↗