Generating human artery and vein cells from pluripotent stem cells highlights the arterial tropism of Nipah and Hendra viruses

Elsevier BV - Tập 185 Số 14 - Trang 2523-2541.e30 - 2022
Lay Teng Lay Teng, Alana T. Alana T., Kevin J. Kevin J., Angela Angela, Xiaochen Xiaochen, Matthew Matthew, Renata M. Renata M., Brian C. Brian C., Chun Yi Chun Yi, Uwe Uwe, Angelika Angelika, Benjamin J. Benjamin J., Jonas L. Jonas L., Alyssa R. Alyssa R., Timothy Timothy, Siva Siva, Fabian P. Fabian P., Toshinobu Toshinobu, Joydeep Joydeep, Matthew H. Matthew H., Hiromitsu Hiromitsu, Christine Christine, Steven C. Steven C., Kristy Kristy, Joseph B. Joseph B., Kyle M. Kyle M.

Tài liệu tham khảo

Aljofan, 2009, Characteristics of Nipah virus and Hendra virus replication in different cell lines and their suitability for antiviral screening, Virus Res., 142, 92, 10.1016/j.virusres.2009.01.014 Andrews Ang, 2018, Nipah virus infection, J. Clin. Microbiol., 56, 10.1128/JCM.01875-17 Aranguren, 2013, Unraveling a novel transcription factor code determining the human arterial-specific endothelial cell signature, Blood, 122, 3982, 10.1182/blood-2013-02-483255 Arunkumar, 2019, Outbreak investigation of Nipah virus disease in Kerala, India, 2018, J. Infect. Dis., 219, 1867, 10.1093/infdis/jiy612 Augustin, 2017, Organotypic vasculature: From descriptive heterogeneity to functional pathophysiology, Science, 357, eaal2379, 10.1126/science.aal2379 Babicki, 2016, Heatmapper: web-enabled heat mapping for all, Nucleic Acids Res., 44, W147, 10.1093/nar/gkw419 Baseler, 2015, Syrian hamsters (Mesocricetus auratus) oronasally inoculated with a Nipah virus isolate from Bangladesh or Malaysia develop similar respiratory tract lesions, Vet. Pathol., 52, 38, 10.1177/0300985814556189 Becht, 2018, Dimensionality reduction for visualizing single-cell data using UMAP, Nat. Biotechnol., 37, 38, 10.1038/nbt.4314 Bonaparte, 2005, Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus, Proc. Natl. Acad. Sci. USA, 102, 10652, 10.1073/pnas.0504887102 Bray, 2016, Near-optimal probabilistic RNA-seq quantification, Nat. Biotechnol., 34, 525, 10.1038/nbt.3519 Cantell, 1981, Preparation and assay of Sendai virus, Methods Enzymol., 78, 299, 10.1016/0076-6879(81)78131-X Carmeliet, 2005, Angiogenesis in life, disease and medicine, Nature, 438, 932, 10.1038/nature04478 Casie Chetty, 2017, Vegf signaling promotes vascular endothelial differentiation by modulating etv2 expression, Dev. Biol., 424, 147, 10.1016/j.ydbio.2017.03.005 2020 Chen, 2013, Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool, BMC Bioinformatics, 14, 128, 10.1186/1471-2105-14-128 Childs, 2007, mda-5, but not RIG-I, is a common target for paramyxovirus V proteins, Virology, 359, 190, 10.1016/j.virol.2006.09.023 Chong, 2011, Stepwise arteriovenous fate acquisition during mammalian vasculogenesis, Dev. Dyn., 240, 2153, 10.1002/dvdy.22706 Chua, 2000, Nipah virus: a recently emergent deadly paramyxovirus, Science, 288, 1432, 10.1126/science.288.5470.1432 Ciancanelli, 2009, Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism, J. Virol., 83, 7828, 10.1128/JVI.02610-08 Ciau-Uitz, 2013, VEGFA-dependent and -independent pathways synergise to drive Scl expression and initiate programming of the blood stem cell lineage in Xenopus, Development, 140, 2632, 10.1242/dev.090829 Corada, 2013, Sox17 is indispensable for acquisition and maintenance of arterial identity, Nat. Commun., 4, 2609, 10.1038/ncomms3609 Coultas, 2005, Endothelial cells and VEGF in vascular development, Nature, 438, 937, 10.1038/nature04479 Cradick, 2014, Cosmid: a web-based tool for identifying and validating CRISPR/Cas off-target sites, Mol. Ther. Nucleic Acids, 3, e214, 10.1038/mtna.2014.64 Davis, 2008, Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors, Blood, 111, 1876, 10.1182/blood-2007-06-093609 de Chaumont, 2012, Icy: an open BioImage informatics platform for extended reproducible research, Nat. Methods, 9, 690, 10.1038/nmeth.2075 De Val, 2009, Transcriptional control of endothelial cell development, Dev. Cell, 16, 180, 10.1016/j.devcel.2009.01.014 DeBuysscher, 2013, Comparison of the pathogenicity of Nipah virus isolates from Bangladesh and Malaysia in the Syrian hamster, PLoS Negl. Trop. Dis., 7, e2024, 10.1371/journal.pntd.0002024 Ditadi, 2015, Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages, Nat. Cell Biol., 17, 580, 10.1038/ncb3161 Drubin, 2017, Stem cells: the new “model organism”, Mol. Biol. Cell, 28, 1409, 10.1091/mbc.e17-03-0183 Duarte, 2004, Dosage-sensitive requirement for mouse Dll4 in artery development, Genes Dev., 18, 2474, 10.1101/gad.1239004 Ellis, 1939, The growth of bacteriophage, J. Gen. Physiol., 22, 365, 10.1085/jgp.22.3.365 Elvert, 2020, Cytokine induction in Nipah virus-infected primary human and porcine bronchial epithelial cells, J. Infect. Dis., 221, S395, 10.1093/infdis/jiz455 Erbar, 2008, Selective receptor expression restricts Nipah virus infection of endothelial cells, Virol. J., 5, 142, 10.1186/1743-422X-5-142 Fang, 2019, Molecular regulation of arteriovenous endothelial cell specification, F1000Res, 8, 1208, 10.12688/f1000research.16701.1 Fish, 2015, The molecular regulation of arteriovenous specification and maintenance, Dev. Dyn., 244, 391, 10.1002/dvdy.24252 Fowler, 2019, A critical look: challenges in differentiating human pluripotent stem cells into desired cell types and organoids, Wiley Interdiscip. Rev.: Dev. Biol., 113 Gage, 2020, Generation of functional liver sinusoidal endothelial cells from human pluripotent stem-cell-derived venous angioblasts, Cell Stem Cell, 27, 254, 10.1016/j.stem.2020.06.007 Gale, 2004, Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development, Proc. Natl. Acad. Sci. USA, 101, 15949, 10.1073/pnas.0407290101 Geisbert, 2010, Development of an acute and highly pathogenic nonhuman primate model of Nipah virus infection, PLoS One, 5, e10690, 10.1371/journal.pone.0010690 Goldstein, 2011, Purification and direct transformation of epithelial progenitor cells from primary human prostate, Nat. Protoc., 6, 656, 10.1038/nprot.2011.317 Gómez Román, 2022, Medical countermeasures against henipaviruses: a review and public health perspective, Lancet Infect. Dis., 22, e13, 10.1016/S1473-3099(21)00400-X Hafemeister, 2019, Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression, Genome Biol., 20, 296, 10.1186/s13059-019-1874-1 Halaidych, 2018, Inflammatory responses and barrier function of endothelial cells derived from human induced pluripotent stem cells, Stem Cell Rep., 10, 1642, 10.1016/j.stemcr.2018.03.012 Harcourt, 2000, Molecular characterization of Nipah virus, a newly emergent paramyxovirus, Virology, 271, 334, 10.1006/viro.2000.0340 Harschnitz, 2021, Human stem cell models to study host-virus interactions in the central nervous system, Nat. Rev. Immunol., 21, 441, 10.1038/s41577-020-00474-y Hong, 2006, Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling, Curr. Biol., 16, 1366, 10.1016/j.cub.2006.05.046 Iwano, 2018, Single-cell bioluminescence imaging of deep tissue in freely moving animals, Science, 359, 935, 10.1126/science.aaq1067 Kälin, 2007, Paracrine and autocrine mechanisms of apelin signaling govern embryonic and tumor angiogenesis, Dev. Biol., 305, 599, 10.1016/j.ydbio.2007.03.004 Kalucka, 2020, Single-cell transcriptome atlas of murine endothelial cells, Cell, 180, 764, 10.1016/j.cell.2020.01.015 Kidoya, 2015, APJ regulates parallel alignment of arteries and veins in the skin, Dev. Cell, 33, 247, 10.1016/j.devcel.2015.02.024 Krebs, 2004, Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants, Genes Dev., 18, 2469, 10.1101/gad.1239204 Krueger Kuleshov, 2016, Enrichr: a comprehensive gene set enrichment analysis web server 2016 update, Nucleic Acids Res., 44, W90, 10.1093/nar/gkw377 Kurian, 2013, Conversion of human fibroblasts to angioblast-like progenitor cells, Nat. Methods, 10, 77, 10.1038/nmeth.2255 Kurokawa, 2017, Human induced pluripotent stem cell-derived endothelial cells for three-dimensional microphysiological systems, Tissue Eng. Part C Methods, 23, 474, 10.1089/ten.tec.2017.0133 Labun, 2019, CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing, Nucleic Acids Res., 47, W171, 10.1093/nar/gkz365 Law, 2014, voom: precision weights unlock linear model analysis tools for RNA-seq read counts, Genome Biol., 15, R29, 10.1186/gb-2014-15-2-r29 Lawson, 2001, Notch signaling is required for arterial-venous differentiation during embryonic vascular development, Development, 128, 3675, 10.1242/dev.128.19.3675 Lawson, 2002, sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation, Dev. Cell, 3, 127, 10.1016/S1534-5807(02)00198-3 Lian, 2014, Efficient differentiation of human pluripotent stem cells to endothelial progenitors via small-molecule activation of WNT signaling, Stem Cell Rep., 3, 804, 10.1016/j.stemcr.2014.09.005 Lin, 2007, Artery and vein formation: a tug of war between different forces, EMBO Rep., 8, 920, 10.1038/sj.embor.7401076 Lin, 2017, Differentiation, evaluation, and application of human induced pluripotent stem cell-derived endothelial cells, Arterioscler. Thromb. Vasc. Biol., 37, 2014, 10.1161/ATVBAHA.117.309962 Lo, 2010, Characterization of the antiviral and inflammatory responses against Nipah virus in endothelial cells and neurons, Virology, 404, 78, 10.1016/j.virol.2010.05.005 Loh, 2014, Efficient endoderm induction from human pluripotent stem cells by logically directing signals controlling lineage bifurcations, Cell Stem Cell, 14, 237, 10.1016/j.stem.2013.12.007 Loh, 2016, Mapping the pairwise choices leading from pluripotency to human bone, heart, and other mesoderm cell types, Cell, 166, 451, 10.1016/j.cell.2016.06.011 López, 2006, Sendai virus infection induces efficient adaptive immunity independently of type I interferons, J. Virol., 80, 4538, 10.1128/JVI.80.9.4538-4545.2006 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Lu, 2004, The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system, Nature, 432, 179, 10.1038/nature03080 Mahalingam, 2012, Hendra virus: an emerging paramyxovirus in Australia, Lancet Infect. Dis., 12, 799, 10.1016/S1473-3099(12)70158-5 Martin, 2019, Highly efficient and marker-free genome editing of human pluripotent stem cells by CRISPR-Cas9 RNP and AAV6 donor-mediated homologous recombination, Cell Stem Cell, 24, 821, 10.1016/j.stem.2019.04.001 Masaki, 2016, Inhibition of apoptosis overcomes stage-related compatibility barriers to chimera formation in mouse embryos, Cell Stem Cell, 19, 587, 10.1016/j.stem.2016.10.013 Mathieu, 2012, Lethal Nipah virus infection induces rapid overexpression of CXCL10, PLoS One, 7, e32157, 10.1371/journal.pone.0032157 McCracken, 2019, Transcriptional dynamics of pluripotent stem cell-derived endothelial cell differentiation revealed by single-cell RNA sequencing, Eur. Heart J., 385, 9963117 Mehand, 2018, The WHO R&D Blueprint: 2018 review of emerging infectious diseases requiring urgent research and development efforts, Antiviral Res., 159, 63, 10.1016/j.antiviral.2018.09.009 Metzger, 2012, MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function, Nature, 484, 120, 10.1038/nature10914 Monaghan, 2014, Detailed morphological characterisation of Hendra virus infection of different cell types using super-resolution and conventional imaging, Virol. J., 11, 200, 10.1186/s12985-014-0200-5 Murray, 1995, A morbillivirus that caused fatal disease in horses and humans, Science, 268, 94, 10.1126/science.7701348 Nakatsu, 2007, Optimized fibrin gel bead assay for the study of angiogenesis, J. Vis. Exp., 3, 186 Negrete, 2007, Single amino acid changes in the Nipah and Hendra virus attachment glycoproteins distinguish ephrinB2 from ephrinB3 usage, J. Virol., 81, 10804, 10.1128/JVI.00999-07 Negrete, 2005, EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus, Nature, 436, 401, 10.1038/nature03838 Ng, 2020, A comprehensive library of human transcription factors for cell fate engineering, Nat. Biotechnol., 51, 987 Nguyen, 2021, The next generation of endothelial differentiation: tissue-specific ECs, Cell Stem Cell, 28, 1188, 10.1016/j.stem.2021.05.002 Nguyen, 2016, Differentiation of human embryonic stem cells to endothelial progenitor cells on laminins in defined and xeno-free systems, Stem Cell Rep., 7, 802, 10.1016/j.stemcr.2016.08.017 Nishimura, 2017, Simple and effective generation of transgene-free induced pluripotent stem cells using an auto-erasable Sendai virus vector responding to microRNA-302, Stem Cell Res., 23, 13, 10.1016/j.scr.2017.06.011 Nishimura, 2011, Development of defective and persistent Sendai virus vector: a unique gene delivery/expression system ideal for cell reprogramming, J. Biol. Chem., 286, 4760, 10.1074/jbc.M110.183780 Olmer, 2018, Differentiation of human pluripotent stem cells into functional endothelial cells in scalable suspension culture, Stem Cell Rep., 10, 1657, 10.1016/j.stemcr.2018.03.017 Ouyang, 2021, ShinyCell: simple and sharable visualisation of single-cell gene expression data, Bioinformatics, btab209 Paik, 2018, Large-scale single-cell RNA-seq reveals molecular signatures of heterogeneous populations of human induced pluripotent stem cell-derived endothelial cells, Circ. Res., 123, 443, 10.1161/CIRCRESAHA.118.312913 Palomares, 2013, Nipah virus envelope-pseudotyped lentiviruses efficiently target ephrinB2-positive stem cell populations in vitro and bypass the liver sink when administered in vivo, J. Virol., 87, 2094, 10.1128/JVI.02032-12 Park, 2018, Activation of the arterial program drives development of definitive hemogenic endothelium with lymphoid potential, Cell Rep., 23, 2467, 10.1016/j.celrep.2018.04.092 Patsch, 2015, Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells, Nat. Cell Biol., 17, 994, 10.1038/ncb3205 Poduri, 2017, Endothelial cells respond to the direction of mechanical stimuli through SMAD signaling to regulate coronary artery size, Development, 144, 3241 Potente, 2017, Vascular heterogeneity and specialization in development and disease, Nat. Rev. Mol. Cell Biol., 18, 477, 10.1038/nrm.2017.36 Prescott, 2015, Single-dose live-attenuated vesicular stomatitis virus-based vaccine protects African green monkeys from Nipah virus disease, Vaccine, 33, 2823, 10.1016/j.vaccine.2015.03.089 Rafii, 2016, Angiocrine functions of organ-specific endothelial cells, Nature, 529, 316, 10.1038/nature17040 Red-Horse, 2019, Veins and arteries Build Hierarchical Branching Patterns Differently: Bottom-Up versus Top-Down, BioEssays, 41, e1800198, 10.1002/bies.201800198 Reich, 2006, GenePattern 2.0, Nat. Genet., 38, 500, 10.1038/ng0506-500 Ritchie, 2015, limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Rodriguez, 2002, Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation, J. Virol., 76, 11476, 10.1128/JVI.76.22.11476-11483.2002 Rosa, 2019, Functional characterization of iPSC-derived arterial- and venous-like endothelial cells, Sci. Rep., 9, 3826, 10.1038/s41598-019-40417-9 Sakamoto, 2007, Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos, Biochem. Biophys. Res. Commun., 360, 539, 10.1016/j.bbrc.2007.06.093 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schountz, 2019, Differential innate immune responses elicited by Nipah virus and cedar virus correlate with disparate in vivo pathogenesis in hamsters, Viruses, 11, 10.3390/v11030291 Shalaby, 1995, Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice, Nature, 376, 62, 10.1038/376062a0 Shaw, 2017, Fundamental properties of the mammalian innate immune system revealed by multispecies comparison of type I interferon responses, PLoS Biol., 15, e2004086, 10.1371/journal.pbio.2004086 Shin, 2008, Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis, Blood, 112, 2318, 10.1182/blood-2008-05-156331 Simoneau, 2020, Modeling multi-organ infection by SARS-CoV-2 using stem cell technology, Cell Stem Cell, 27, 859, 10.1016/j.stem.2020.11.012 Sriram, 2015, Efficient differentiation of human embryonic stem cells to arterial and venous endothelial cells under feeder- and serum- free conditions, Stem Cell Res. Ther., 6, 261, 10.1186/s13287-015-0260-5 Stuart, 2019, Comprehensive integration of single-cell data, Cell, 177, 1888, 10.1016/j.cell.2019.05.031 Tai-Nagara, 2017, Placental labyrinth formation in mice requires endothelial FLRT2/UNC5B signaling, Development, 144, 2392 Takashima, 2014, Resetting transcription factor control circuitry toward ground-state pluripotency in human, Cell, 158, 1254, 10.1016/j.cell.2014.08.029 Tinevez, 2017, TrackMate: an open and extensible platform for single-particle tracking, Methods, 115, 80, 10.1016/j.ymeth.2016.09.016 Travaglini, 2020, A molecular cell atlas of the human lung from single-cell RNA sequencing, Nature, 587, 619, 10.1038/s41586-020-2922-4 Virtue, 2011, Interferon signaling remains functional during Henipavirus infection of human cell lines, J. Virol., 85, 4031, 10.1128/JVI.02412-10 Wang, 1998, Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4, Cell, 93, 741, 10.1016/S0092-8674(00)81436-1 Wang, 2020, Robust differentiation of human pluripotent stem cells into endothelial cells via temporal modulation of ETV2 with modified mRNA, Sci. Adv., 6, eaba7606, 10.1126/sciadv.aba7606 Wickham, 2016 Wickham, 2019, Welcome to the Tidyverse, J. Open Source Software, 4 Wickham Wong, 2002, Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis, Am. J. Pathol., 161, 2153, 10.1016/S0002-9440(10)64493-8 Xu, 2014, Arteries are formed by vein-derived endothelial tip cells, Nat. Commun., 5, 5758, 10.1038/ncomms6758 Yoshida, 2018, A single amino acid substitution within the paramyxovirus Sendai virus nucleoprotein is a critical determinant for production of interferon-beta-inducing copyback-type defective interfering genomes, J. Virol., 92, 10.1128/JVI.02094-17 Zeng, 2019, Tracing the first hematopoietic stem cell generation in human embryo by single-cell RNA sequencing, Cell Res., 29, 881, 10.1038/s41422-019-0228-6 Zhang, 2017, 201702295 Zheng, 2017, Massively parallel digital transcriptional profiling of single cells, Nat. Commun., 8, 14049, 10.1038/ncomms14049