Cargando…

A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2

The SARS-CoV-2 pandemic has caused over 1 million deaths globally, mostly due to acute lung injury and acute respiratory distress syndrome, or direct complications resulting in multiple-organ failures. Little is known about the host tissue immune and cellular responses associated with COVID-19 infec...

Descripción completa

Detalles Bibliográficos
Autores principales: Delorey, Toni M., Ziegler, Carly G. K., Heimberg, Graham, Normand, Rachelly, Yang, Yiming, Segerstolpe, Asa, Abbondanza, Domenic, Fleming, Stephen J., Subramanian, Ayshwarya, Montoro, Daniel T., Jagadeesh, Karthik A., Dey, Kushal K., Sen, Pritha, Slyper, Michal, Pita-Juárez, Yered H., Phillips, Devan, Bloom-Ackerman, Zohar, Barkas, Nick, Ganna, Andrea, Gomez, James, Normandin, Erica, Naderi, Pourya, Popov, Yury V., Raju, Siddharth S., Niezen, Sebastian, Tsai, Linus T.-Y., Siddle, Katherine J., Sud, Malika, Tran, Victoria M., Vellarikkal, Shamsudheen K., Amir-Zilberstein, Liat, Atri, Deepak S., Beechem, Joseph, Brook, Olga R., Chen, Jonathan, Divakar, Prajan, Dorceus, Phylicia, Engreitz, Jesse M., Essene, Adam, Fitzgerald, Donna M., Fropf, Robin, Gazal, Steven, Gould, Joshua, Grzyb, John, Harvey, Tyler, Hecht, Jonathan, Hether, Tyler, Jane-Valbuena, Judit, Leney-Greene, Michael, Ma, Hui, McCabe, Cristin, McLoughlin, Daniel E., Miller, Eric M., Muus, Christoph, Niemi, Mari, Padera, Robert, Pan, Liuliu, Pant, Deepti, Pe’er, Carmel, Pfiffner-Borges, Jenna, Pinto, Christopher J., Plaisted, Jacob, Reeves, Jason, Ross, Marty, Rudy, Melissa, Rueckert, Erroll H., Siciliano, Michelle, Sturm, Alexander, Todres, Ellen, Waghray, Avinash, Warren, Sarah, Zhang, Shuting, Zollinger, Daniel R., Cosimi, Lisa, Gupta, Rajat M., Hacohen, Nir, Hide, Winston, Price, Alkes L., Rajagopal, Jayaraj, Tata, Purushothama Rao, Riedel, Stefan, Szabo, Gyongyi, Tickle, Timothy L., Hung, Deborah, Sabeti, Pardis C., Novak, Richard, Rogers, Robert, Ingber, Donald E., Jiang, Z. Gordon, Juric, Dejan, Babadi, Mehrtash, Farhi, Samouil L., Stone, James R., Vlachos, Ioannis S., Solomon, Isaac H., Ashenberg, Orr, Porter, Caroline B.M., Li, Bo, Shalek, Alex K., Villani, Alexandra-Chloé, Rozenblatt-Rosen, Orit, Regev, Aviv
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924267/
https://www.ncbi.nlm.nih.gov/pubmed/33655247
http://dx.doi.org/10.1101/2021.02.25.430130
_version_ 1783659054846967808
author Delorey, Toni M.
Ziegler, Carly G. K.
Heimberg, Graham
Normand, Rachelly
Yang, Yiming
Segerstolpe, Asa
Abbondanza, Domenic
Fleming, Stephen J.
Subramanian, Ayshwarya
Montoro, Daniel T.
Jagadeesh, Karthik A.
Dey, Kushal K.
Sen, Pritha
Slyper, Michal
Pita-Juárez, Yered H.
Phillips, Devan
Bloom-Ackerman, Zohar
Barkas, Nick
Ganna, Andrea
Gomez, James
Normandin, Erica
Naderi, Pourya
Popov, Yury V.
Raju, Siddharth S.
Niezen, Sebastian
Tsai, Linus T.-Y.
Siddle, Katherine J.
Sud, Malika
Tran, Victoria M.
Vellarikkal, Shamsudheen K.
Amir-Zilberstein, Liat
Atri, Deepak S.
Beechem, Joseph
Brook, Olga R.
Chen, Jonathan
Divakar, Prajan
Dorceus, Phylicia
Engreitz, Jesse M.
Essene, Adam
Fitzgerald, Donna M.
Fropf, Robin
Gazal, Steven
Gould, Joshua
Grzyb, John
Harvey, Tyler
Hecht, Jonathan
Hether, Tyler
Jane-Valbuena, Judit
Leney-Greene, Michael
Ma, Hui
McCabe, Cristin
McLoughlin, Daniel E.
Miller, Eric M.
Muus, Christoph
Niemi, Mari
Padera, Robert
Pan, Liuliu
Pant, Deepti
Pe’er, Carmel
Pfiffner-Borges, Jenna
Pinto, Christopher J.
Plaisted, Jacob
Reeves, Jason
Ross, Marty
Rudy, Melissa
Rueckert, Erroll H.
Siciliano, Michelle
Sturm, Alexander
Todres, Ellen
Waghray, Avinash
Warren, Sarah
Zhang, Shuting
Zollinger, Daniel R.
Cosimi, Lisa
Gupta, Rajat M.
Hacohen, Nir
Hide, Winston
Price, Alkes L.
Rajagopal, Jayaraj
Tata, Purushothama Rao
Riedel, Stefan
Szabo, Gyongyi
Tickle, Timothy L.
Hung, Deborah
Sabeti, Pardis C.
Novak, Richard
Rogers, Robert
Ingber, Donald E.
Jiang, Z. Gordon
Juric, Dejan
Babadi, Mehrtash
Farhi, Samouil L.
Stone, James R.
Vlachos, Ioannis S.
Solomon, Isaac H.
Ashenberg, Orr
Porter, Caroline B.M.
Li, Bo
Shalek, Alex K.
Villani, Alexandra-Chloé
Rozenblatt-Rosen, Orit
Regev, Aviv
author_facet Delorey, Toni M.
Ziegler, Carly G. K.
Heimberg, Graham
Normand, Rachelly
Yang, Yiming
Segerstolpe, Asa
Abbondanza, Domenic
Fleming, Stephen J.
Subramanian, Ayshwarya
Montoro, Daniel T.
Jagadeesh, Karthik A.
Dey, Kushal K.
Sen, Pritha
Slyper, Michal
Pita-Juárez, Yered H.
Phillips, Devan
Bloom-Ackerman, Zohar
Barkas, Nick
Ganna, Andrea
Gomez, James
Normandin, Erica
Naderi, Pourya
Popov, Yury V.
Raju, Siddharth S.
Niezen, Sebastian
Tsai, Linus T.-Y.
Siddle, Katherine J.
Sud, Malika
Tran, Victoria M.
Vellarikkal, Shamsudheen K.
Amir-Zilberstein, Liat
Atri, Deepak S.
Beechem, Joseph
Brook, Olga R.
Chen, Jonathan
Divakar, Prajan
Dorceus, Phylicia
Engreitz, Jesse M.
Essene, Adam
Fitzgerald, Donna M.
Fropf, Robin
Gazal, Steven
Gould, Joshua
Grzyb, John
Harvey, Tyler
Hecht, Jonathan
Hether, Tyler
Jane-Valbuena, Judit
Leney-Greene, Michael
Ma, Hui
McCabe, Cristin
McLoughlin, Daniel E.
Miller, Eric M.
Muus, Christoph
Niemi, Mari
Padera, Robert
Pan, Liuliu
Pant, Deepti
Pe’er, Carmel
Pfiffner-Borges, Jenna
Pinto, Christopher J.
Plaisted, Jacob
Reeves, Jason
Ross, Marty
Rudy, Melissa
Rueckert, Erroll H.
Siciliano, Michelle
Sturm, Alexander
Todres, Ellen
Waghray, Avinash
Warren, Sarah
Zhang, Shuting
Zollinger, Daniel R.
Cosimi, Lisa
Gupta, Rajat M.
Hacohen, Nir
Hide, Winston
Price, Alkes L.
Rajagopal, Jayaraj
Tata, Purushothama Rao
Riedel, Stefan
Szabo, Gyongyi
Tickle, Timothy L.
Hung, Deborah
Sabeti, Pardis C.
Novak, Richard
Rogers, Robert
Ingber, Donald E.
Jiang, Z. Gordon
Juric, Dejan
Babadi, Mehrtash
Farhi, Samouil L.
Stone, James R.
Vlachos, Ioannis S.
Solomon, Isaac H.
Ashenberg, Orr
Porter, Caroline B.M.
Li, Bo
Shalek, Alex K.
Villani, Alexandra-Chloé
Rozenblatt-Rosen, Orit
Regev, Aviv
author_sort Delorey, Toni M.
collection PubMed
description The SARS-CoV-2 pandemic has caused over 1 million deaths globally, mostly due to acute lung injury and acute respiratory distress syndrome, or direct complications resulting in multiple-organ failures. Little is known about the host tissue immune and cellular responses associated with COVID-19 infection, symptoms, and lethality. To address this, we collected tissues from 11 organs during the clinical autopsy of 17 individuals who succumbed to COVID-19, resulting in a tissue bank of approximately 420 specimens. We generated comprehensive cellular maps capturing COVID-19 biology related to patients’ demise through single-cell and single-nucleus RNA-Seq of lung, kidney, liver and heart tissues, and further contextualized our findings through spatial RNA profiling of distinct lung regions. We developed a computational framework that incorporates removal of ambient RNA and automated cell type annotation to facilitate comparison with other healthy and diseased tissue atlases. In the lung, we uncovered significantly altered transcriptional programs within the epithelial, immune, and stromal compartments and cell intrinsic changes in multiple cell types relative to lung tissue from healthy controls. We observed evidence of: alveolar type 2 (AT2) differentiation replacing depleted alveolar type 1 (AT1) lung epithelial cells, as previously seen in fibrosis; a concomitant increase in myofibroblasts reflective of defective tissue repair; and, putative TP63(+) intrapulmonary basal-like progenitor (IPBLP) cells, similar to cells identified in H1N1 influenza, that may serve as an emergency cellular reserve for severely damaged alveoli. Together, these findings suggest the activation and failure of multiple avenues for regeneration of the epithelium in these terminal lungs. SARS-CoV-2 RNA reads were enriched in lung mononuclear phagocytic cells and endothelial cells, and these cells expressed distinct host response transcriptional programs. We corroborated the compositional and transcriptional changes in lung tissue through spatial analysis of RNA profiles in situ and distinguished unique tissue host responses between regions with and without viral RNA, and in COVID-19 donor tissues relative to healthy lung. Finally, we analyzed genetic regions implicated in COVID-19 GWAS with transcriptomic data to implicate specific cell types and genes associated with disease severity. Overall, our COVID-19 cell atlas is a foundational dataset to better understand the biological impact of SARS-CoV-2 infection across the human body and empowers the identification of new therapeutic interventions and prevention strategies.
format Online
Article
Text
id pubmed-7924267
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-79242672021-03-03 A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2 Delorey, Toni M. Ziegler, Carly G. K. Heimberg, Graham Normand, Rachelly Yang, Yiming Segerstolpe, Asa Abbondanza, Domenic Fleming, Stephen J. Subramanian, Ayshwarya Montoro, Daniel T. Jagadeesh, Karthik A. Dey, Kushal K. Sen, Pritha Slyper, Michal Pita-Juárez, Yered H. Phillips, Devan Bloom-Ackerman, Zohar Barkas, Nick Ganna, Andrea Gomez, James Normandin, Erica Naderi, Pourya Popov, Yury V. Raju, Siddharth S. Niezen, Sebastian Tsai, Linus T.-Y. Siddle, Katherine J. Sud, Malika Tran, Victoria M. Vellarikkal, Shamsudheen K. Amir-Zilberstein, Liat Atri, Deepak S. Beechem, Joseph Brook, Olga R. Chen, Jonathan Divakar, Prajan Dorceus, Phylicia Engreitz, Jesse M. Essene, Adam Fitzgerald, Donna M. Fropf, Robin Gazal, Steven Gould, Joshua Grzyb, John Harvey, Tyler Hecht, Jonathan Hether, Tyler Jane-Valbuena, Judit Leney-Greene, Michael Ma, Hui McCabe, Cristin McLoughlin, Daniel E. Miller, Eric M. Muus, Christoph Niemi, Mari Padera, Robert Pan, Liuliu Pant, Deepti Pe’er, Carmel Pfiffner-Borges, Jenna Pinto, Christopher J. Plaisted, Jacob Reeves, Jason Ross, Marty Rudy, Melissa Rueckert, Erroll H. Siciliano, Michelle Sturm, Alexander Todres, Ellen Waghray, Avinash Warren, Sarah Zhang, Shuting Zollinger, Daniel R. Cosimi, Lisa Gupta, Rajat M. Hacohen, Nir Hide, Winston Price, Alkes L. Rajagopal, Jayaraj Tata, Purushothama Rao Riedel, Stefan Szabo, Gyongyi Tickle, Timothy L. Hung, Deborah Sabeti, Pardis C. Novak, Richard Rogers, Robert Ingber, Donald E. Jiang, Z. Gordon Juric, Dejan Babadi, Mehrtash Farhi, Samouil L. Stone, James R. Vlachos, Ioannis S. Solomon, Isaac H. Ashenberg, Orr Porter, Caroline B.M. Li, Bo Shalek, Alex K. Villani, Alexandra-Chloé Rozenblatt-Rosen, Orit Regev, Aviv bioRxiv Article The SARS-CoV-2 pandemic has caused over 1 million deaths globally, mostly due to acute lung injury and acute respiratory distress syndrome, or direct complications resulting in multiple-organ failures. Little is known about the host tissue immune and cellular responses associated with COVID-19 infection, symptoms, and lethality. To address this, we collected tissues from 11 organs during the clinical autopsy of 17 individuals who succumbed to COVID-19, resulting in a tissue bank of approximately 420 specimens. We generated comprehensive cellular maps capturing COVID-19 biology related to patients’ demise through single-cell and single-nucleus RNA-Seq of lung, kidney, liver and heart tissues, and further contextualized our findings through spatial RNA profiling of distinct lung regions. We developed a computational framework that incorporates removal of ambient RNA and automated cell type annotation to facilitate comparison with other healthy and diseased tissue atlases. In the lung, we uncovered significantly altered transcriptional programs within the epithelial, immune, and stromal compartments and cell intrinsic changes in multiple cell types relative to lung tissue from healthy controls. We observed evidence of: alveolar type 2 (AT2) differentiation replacing depleted alveolar type 1 (AT1) lung epithelial cells, as previously seen in fibrosis; a concomitant increase in myofibroblasts reflective of defective tissue repair; and, putative TP63(+) intrapulmonary basal-like progenitor (IPBLP) cells, similar to cells identified in H1N1 influenza, that may serve as an emergency cellular reserve for severely damaged alveoli. Together, these findings suggest the activation and failure of multiple avenues for regeneration of the epithelium in these terminal lungs. SARS-CoV-2 RNA reads were enriched in lung mononuclear phagocytic cells and endothelial cells, and these cells expressed distinct host response transcriptional programs. We corroborated the compositional and transcriptional changes in lung tissue through spatial analysis of RNA profiles in situ and distinguished unique tissue host responses between regions with and without viral RNA, and in COVID-19 donor tissues relative to healthy lung. Finally, we analyzed genetic regions implicated in COVID-19 GWAS with transcriptomic data to implicate specific cell types and genes associated with disease severity. Overall, our COVID-19 cell atlas is a foundational dataset to better understand the biological impact of SARS-CoV-2 infection across the human body and empowers the identification of new therapeutic interventions and prevention strategies. Cold Spring Harbor Laboratory 2021-02-25 /pmc/articles/PMC7924267/ /pubmed/33655247 http://dx.doi.org/10.1101/2021.02.25.430130 Text en https://creativecommons.org/licenses/by-nd/4.0/This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Delorey, Toni M.
Ziegler, Carly G. K.
Heimberg, Graham
Normand, Rachelly
Yang, Yiming
Segerstolpe, Asa
Abbondanza, Domenic
Fleming, Stephen J.
Subramanian, Ayshwarya
Montoro, Daniel T.
Jagadeesh, Karthik A.
Dey, Kushal K.
Sen, Pritha
Slyper, Michal
Pita-Juárez, Yered H.
Phillips, Devan
Bloom-Ackerman, Zohar
Barkas, Nick
Ganna, Andrea
Gomez, James
Normandin, Erica
Naderi, Pourya
Popov, Yury V.
Raju, Siddharth S.
Niezen, Sebastian
Tsai, Linus T.-Y.
Siddle, Katherine J.
Sud, Malika
Tran, Victoria M.
Vellarikkal, Shamsudheen K.
Amir-Zilberstein, Liat
Atri, Deepak S.
Beechem, Joseph
Brook, Olga R.
Chen, Jonathan
Divakar, Prajan
Dorceus, Phylicia
Engreitz, Jesse M.
Essene, Adam
Fitzgerald, Donna M.
Fropf, Robin
Gazal, Steven
Gould, Joshua
Grzyb, John
Harvey, Tyler
Hecht, Jonathan
Hether, Tyler
Jane-Valbuena, Judit
Leney-Greene, Michael
Ma, Hui
McCabe, Cristin
McLoughlin, Daniel E.
Miller, Eric M.
Muus, Christoph
Niemi, Mari
Padera, Robert
Pan, Liuliu
Pant, Deepti
Pe’er, Carmel
Pfiffner-Borges, Jenna
Pinto, Christopher J.
Plaisted, Jacob
Reeves, Jason
Ross, Marty
Rudy, Melissa
Rueckert, Erroll H.
Siciliano, Michelle
Sturm, Alexander
Todres, Ellen
Waghray, Avinash
Warren, Sarah
Zhang, Shuting
Zollinger, Daniel R.
Cosimi, Lisa
Gupta, Rajat M.
Hacohen, Nir
Hide, Winston
Price, Alkes L.
Rajagopal, Jayaraj
Tata, Purushothama Rao
Riedel, Stefan
Szabo, Gyongyi
Tickle, Timothy L.
Hung, Deborah
Sabeti, Pardis C.
Novak, Richard
Rogers, Robert
Ingber, Donald E.
Jiang, Z. Gordon
Juric, Dejan
Babadi, Mehrtash
Farhi, Samouil L.
Stone, James R.
Vlachos, Ioannis S.
Solomon, Isaac H.
Ashenberg, Orr
Porter, Caroline B.M.
Li, Bo
Shalek, Alex K.
Villani, Alexandra-Chloé
Rozenblatt-Rosen, Orit
Regev, Aviv
A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title_full A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title_fullStr A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title_full_unstemmed A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title_short A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2
title_sort single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of sars-cov-2
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924267/
https://www.ncbi.nlm.nih.gov/pubmed/33655247
http://dx.doi.org/10.1101/2021.02.25.430130
work_keys_str_mv AT deloreytonim asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zieglercarlygk asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT heimberggraham asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT normandrachelly asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT yangyiming asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT segerstolpeasa asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT abbondanzadomenic asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT flemingstephenj asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT subramanianayshwarya asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT montorodanielt asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT jagadeeshkarthika asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT deykushalk asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT senpritha asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT slypermichal asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pitajuarezyeredh asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT phillipsdevan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT bloomackermanzohar asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT barkasnick asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gannaandrea asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gomezjames asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT normandinerica asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT naderipourya asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT popovyuryv asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rajusiddharths asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT niezensebastian asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tsailinusty asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT siddlekatherinej asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sudmalika asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tranvictoriam asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT vellarikkalshamsudheenk asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT amirzilbersteinliat asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT atrideepaks asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT beechemjoseph asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT brookolgar asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT chenjonathan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT divakarprajan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT dorceusphylicia asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT engreitzjessem asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT esseneadam asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT fitzgeralddonnam asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT fropfrobin asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gazalsteven asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gouldjoshua asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT grzybjohn asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT harveytyler asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hechtjonathan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hethertyler asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT janevalbuenajudit asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT leneygreenemichael asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mahui asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mccabecristin asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mcloughlindaniele asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT millerericm asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT muuschristoph asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT niemimari asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT paderarobert asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT panliuliu asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pantdeepti asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT peercarmel asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pfiffnerborgesjenna asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pintochristopherj asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT plaistedjacob asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT reevesjason asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rossmarty asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rudymelissa asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rueckerterrollh asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sicilianomichelle asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sturmalexander asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT todresellen asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT waghrayavinash asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT warrensarah asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zhangshuting asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zollingerdanielr asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT cosimilisa asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT guptarajatm asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hacohennir asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hidewinston asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pricealkesl asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rajagopaljayaraj asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tatapurushothamarao asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT riedelstefan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT szabogyongyi asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tickletimothyl asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hungdeborah asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sabetipardisc asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT novakrichard asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rogersrobert asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT ingberdonalde asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT jiangzgordon asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT juricdejan asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT babadimehrtash asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT farhisamouill asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT stonejamesr asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT vlachosioanniss asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT solomonisaach asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT ashenbergorr asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT portercarolinebm asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT libo asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT shalekalexk asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT villanialexandrachloe asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rozenblattrosenorit asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT regevaviv asinglecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT deloreytonim singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zieglercarlygk singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT heimberggraham singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT normandrachelly singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT yangyiming singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT segerstolpeasa singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT abbondanzadomenic singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT flemingstephenj singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT subramanianayshwarya singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT montorodanielt singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT jagadeeshkarthika singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT deykushalk singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT senpritha singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT slypermichal singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pitajuarezyeredh singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT phillipsdevan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT bloomackermanzohar singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT barkasnick singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gannaandrea singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gomezjames singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT normandinerica singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT naderipourya singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT popovyuryv singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rajusiddharths singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT niezensebastian singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tsailinusty singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT siddlekatherinej singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sudmalika singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tranvictoriam singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT vellarikkalshamsudheenk singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT amirzilbersteinliat singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT atrideepaks singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT beechemjoseph singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT brookolgar singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT chenjonathan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT divakarprajan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT dorceusphylicia singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT engreitzjessem singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT esseneadam singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT fitzgeralddonnam singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT fropfrobin singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gazalsteven singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT gouldjoshua singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT grzybjohn singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT harveytyler singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hechtjonathan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hethertyler singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT janevalbuenajudit singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT leneygreenemichael singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mahui singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mccabecristin singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT mcloughlindaniele singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT millerericm singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT muuschristoph singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT niemimari singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT paderarobert singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT panliuliu singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pantdeepti singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT peercarmel singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pfiffnerborgesjenna singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pintochristopherj singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT plaistedjacob singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT reevesjason singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rossmarty singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rudymelissa singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rueckerterrollh singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sicilianomichelle singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sturmalexander singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT todresellen singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT waghrayavinash singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT warrensarah singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zhangshuting singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT zollingerdanielr singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT cosimilisa singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT guptarajatm singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hacohennir singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hidewinston singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT pricealkesl singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rajagopaljayaraj singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tatapurushothamarao singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT riedelstefan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT szabogyongyi singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT tickletimothyl singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT hungdeborah singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT sabetipardisc singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT novakrichard singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rogersrobert singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT ingberdonalde singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT jiangzgordon singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT juricdejan singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT babadimehrtash singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT farhisamouill singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT stonejamesr singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT vlachosioanniss singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT solomonisaach singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT ashenbergorr singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT portercarolinebm singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT libo singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT shalekalexk singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT villanialexandrachloe singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT rozenblattrosenorit singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2
AT regevaviv singlecellandspatialatlasofautopsytissuesrevealspathologyandcellulartargetsofsarscov2