Single cell approach to study host/enteric virus interaction in human mini-gut organoids

• Applicant: Megan Stanifer, Ph.D.
• Subject Area: Virology
• Term: from 2019 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 416072091

• Final Report Year: 2023

No abstract available

Publications

• Asymmetric distribution of TLR3 leads to a polarized immune response in human intestinal epithelial cells. Nature Microbiology, 5(1), 181-191.
  Stanifer, Megan L.; Mukenhirn, Markus; Muenchau, Stephanie; Pervolaraki, Kalliopi; Kanaya, Takashi; Albrecht, Dorothee; Odendall, Charlotte; Hielscher, Thomas; Haucke, Volker; Kagan, Jonathan C.; Bartfeld, Sina; Ohno, Hiroshi & Boulant, Steeve
  
• 3D Correlative Cryo-Structured Illumination Fluorescence and Soft X-ray Microscopy Elucidates Reovirus Intracellular Release Pathway. Cell, 182(2), 515-530.e17.
  Kounatidis, Ilias; Stanifer, Megan L.; Phillips, Michael A.; Paul-Gilloteaux, Perrine; Heiligenstein, Xavier; Wang, Hongchang; Okolo, Chidinma A.; Fish, Thomas M.; Spink, Matthew C.; Stuart, David I.; Davis, Ilan; Boulant, Steeve; Grimes, Jonathan M.; Dobbie, Ian M. & Harkiolaki, Maria
  
• Critical Role of Type III Interferon in Controlling SARS-CoV-2 Infection in Human Intestinal Epithelial Cells. Cell Reports, 32(1), 107863.
  Stanifer, Megan L.; Kee, Carmon; Cortese, Mirko; Zumaran, Camila Metz; Triana, Sergio; Mukenhirn, Markus; Kraeusslich, Hans-Georg; Alexandrov, Theodore; Bartenschlager, Ralf & Boulant, Steeve
  
• Development of Feline Ileum- and Colon-Derived Organoids and Their Potential Use to Support Feline Coronavirus Infection. Cells, 9(9), 2085.
  Tekes, Gergely; Ehmann, Rosina; Boulant, Steeve & Stanifer, Megan L.
  
• Enhanced Uptake and Endosomal Release of LbL Microcarriers Functionalized with Reversible Fusion Proteins. ACS Applied Bio Materials, 3(3), 1553-1567.
  Scheffler, Kira; Bilz, Nicole C.; Brueckner, Mandy; Stanifer, Megan L.; Boulant, Steeve; Claus, Claudia & Reibetanz, Uta
  
• Integrative Imaging Reveals SARS-CoV-2-Induced Reshaping of Subcellular Morphologies. Cell Host & Microbe, 28(6), 853-866.e5.
  Cortese, Mirko; Lee, Ji-Young; Cerikan, Berati; Neufeldt, Christopher J.; Oorschot, Viola M.J.; Köhrer, Sebastian; Hennies, Julian; Schieber, Nicole L.; Ronchi, Paolo; Mizzon, Giulia; Romero-Brey, Inés; Santarella-Mellwig, Rachel; Schorb, Martin; Boermel, Mandy; Mocaer, Karel; Beckwith, Marianne S.; Templin, Rachel M.; Gross, Viktoriia; Pape, Constantin; ... & Bartenschlager, Ralf
  
• Interferons and viruses induce a novel truncated ACE2 isoform and not the full-length SARS-CoV-2 receptor. Nature Genetics, 52(12), 1283-1293.
  Onabajo, Olusegun O.; Banday, A. Rouf; Stanifer, Megan L.; Yan, Wusheng; Obajemu, Adeola; Santer, Deanna M.; Florez-Vargas, Oscar; Piontkivska, Helen; Vargas, Joselin M.; Ring, Timothy J.; Kee, Carmon; Doldan, Patricio; Tyrrell, D. Lorne; Mendoza, Juan L.; Boulant, Steeve & Prokunina-Olsson, Ludmila
  
• Novel Toscana Virus Reverse Genetics System Establishes NSs as an Antagonist of Type I Interferon Responses. Viruses, 12(4), 400.
  Woelfl, Franziska; Léger, Psylvia; Oreshkova, Nadia; Pahmeier, Felix; Windhaber, Stefan; Koch, Jana; Stanifer, Megan; Roman, Sosa Gleyder; Uckeley, Zina M.; Rey, Felix A.; Boulant, Steeve; Kortekaas, Jeroen; Wichgers, Schreur Paul J. & Lozach, Pierre-Yves
  
• SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography. Nature Communications, 11(1).
  Klein, Steffen; Cortese, Mirko; Winter, Sophie L.; Wachsmuth-Melm, Moritz; Neufeldt, Christopher J.; Cerikan, Berati; Stanifer, Megan L.; Boulant, Steeve; Bartenschlager, Ralf & Chlanda, Petr
  
• Adapting Gastrointestinal Organoids for Pathogen Infection and Single Cell Sequencing under Biosafety Level 3 (BSL-3) Conditions. Journal of Visualized Experiments (175).
  Stanifer, Megan L. & Boulant, Steeve
  
• Conserved Induction of Distinct Antiviral Signalling Kinetics by Primate Interferon Lambda 4 Proteins. Frontiers in Immunology, 12 (2021, 11, 18).
  Guo, Cuncai; Reuss, Dorothee; Coey, Jonathon D.; Sukumar, Swathi; Lang, Benjamin; McLauchlan, John; Boulant, Steeve; Stanifer, Megan L. & Bamford, Connor G. G.
  
• Functional comparison of MERS-coronavirus lineages reveals increased replicative fitness of the recombinant lineage 5. Nature Communications, 12(1).
  Schroeder, Simon; Mache, Christin; Kleine-Weber, Hannah; Corman, Victor M.; Muth, Doreen; Richter, Anja; Fatykhova, Diana; Memish, Ziad A.; Stanifer, Megan L.; Boulant, Steeve; Gultom, Mitra; Dijkman, Ronald; Eggeling, Stephan; Hocke, Andreas; Hippenstiel, Stefan; Thiel, Volker; Pöhlmann, Stefan; Wolff, Thorsten; Müller, Marcel A. & Drosten, Christian
  
• Invasiveness of Escherichia coli Is Associated with an IncFII Plasmid. Pathogens, 10(12), 1645.
  Krall, Lars Johannes; Klein, Sabrina; Boutin, Sébastien; Wu, Chia Ching; Sähr, Aline; Stanifer, Megan L.; Boulant, Steeve; Heeg, Klaus; Nurjadi, Dennis & Hildebrand, Dagmar
  
• Single‐cell analyses reveal SARS‐CoV‐2 interference with intrinsic immune response in the human gut. Molecular Systems Biology, 17(4).
  Triana, Sergio; Metz‐Zumaran, Camila; Ramirez, Carlos; Kee, Carmon; Doldan, Patricio; Shahraz, Mohammed; Schraivogel, Daniel; Gschwind, Andreas R.; Sharma, Ashwini K.; Steinmetz, Lars M.; Herrmann, Carl; Alexandrov, Theodore; Boulant, Steeve & Stanifer, Megan L.
  
• Single‐cell transcriptomics reveals immune response of intestinal cell types to viral infection. Molecular Systems Biology, 17(7).
  Triana, Sergio; Stanifer, Megan L; Metz‐Zumaran, Camila; Shahraz, Mohammed; Mukenhirn, Markus; Kee, Carmon; Serger, Clara; Koschny, Ronald; Ordoñez‐Rueda, Diana; Paulsen, Malte; Benes, Vladimir; Boulant, Steeve & Alexandrov, Theodore
  
• The endogenous cellular protease inhibitor SPINT2 controls SARS-CoV-2 viral infection and is associated to disease severity. PLOS Pathogens, 17(6), e1009687.
  Ramirez, Alvarez Carlos; Kee, Carmon; Sharma, Ashwini Kumar; Thomas, Leonie; Schmidt, Florian I.; Stanifer, Megan L.; Boulant, Steeve & Herrmann, Carl
  
• A diabetic milieu increases ACE2 expression and cellular susceptibility to SARS-CoV-2 infections in human kidney organoids and patient cells. Cell Metabolism, 34(6), 857-873.e9.
  Garreta, Elena; Prado, Patricia; Stanifer, Megan L.; Monteil, Vanessa; Marco, Andrés; Ullate-Agote, Asier; Moya-Rull, Daniel; Vilas-Zornoza, Amaia; Tarantino, Carolina; Romero, Juan Pablo; Jonsson, Gustav; Oria, Roger; Leopoldi, Alexandra; Hagelkruys, Astrid; Gallo, Maria; González, Federico; Domingo-Pedrol, Pere; Gavaldà, Aleix; del, Pozo Carmen Hurtado; ... & Montserrat, Nuria
  
• A model for network-based identification and pharmacological targeting of aberrant, replication-permissive transcriptional programs induced by viral infection. Communications Biology, 5(1).
  Laise, Pasquale; Stanifer, Megan L.; Bosker, Gideon; Sun, Xiaoyun; Triana, Sergio; Doldan, Patricio; La Manna, Federico; De Menna, Marta; Realubit, Ronald B.; Pampou, Sergey; Karan, Charles; Alexandrov, Theodore; Kruithof-de, Julio Marianna; Califano, Andrea; Boulant, Steeve & Alvarez, Mariano J.
  
• Ex vivo and in vivo suppression of SARS-CoV-2 with combinatorial AAV/RNAi expression vectors. Molecular Therapy, 30(5), 2005-2023.
  Becker, Jonas; Stanifer, Megan Lynn; Leist, Sarah Rebecca; Stolp, Bettina; Maiakovska, Olena; West, Ande; Wiedtke, Ellen; Börner, Kathleen; Ghanem, Ali; Ambiel, Ina; Tse, Longping Victor; Fackler, Oliver Till; Baric, Ralph Steven; Boulant, Steeve & Grimm, Dirk
  
• Genetic regulation of OAS1 nonsense-mediated decay underlies association with COVID-19 hospitalization in patients of European and African ancestries. Nature Genetics, 54(8), 1103-1116.
  Banday, A. Rouf; Stanifer, Megan L.; Florez-Vargas, Oscar; Onabajo, Olusegun O.; Papenberg, Brenen W.; Zahoor, Muhammad A.; Mirabello, Lisa; Ring, Timothy J.; Lee, Chia-Han; Albert, Paul S.; Andreakos, Evangelos; Arons, Evgeny; Barsh, Greg; Biesecker, Leslie G.; Boyle, David L.; Brahier, Mark S.; Burnett-Hartman, Andrea; Carrington, Mary; Chang, Euijin; ... & Prokunina-Olsson, Ludmila
  
• Increased Sensitivity of SARS-CoV-2 to Type III Interferon in Human Intestinal Epithelial Cells. Journal of Virology, 96(7).
  Metz-Zumaran, Camila; Kee, Carmon; Doldan, Patricio; Guo, Cuncai; Stanifer, Megan L. & Boulant, Steeve
  
• Mapping the epithelial–immune cell interactome upon infection in the gut and the upper airways. npj Systems Biology and Applications, 8(1).
  Poletti, Martina; Treveil, Agatha; Csabai, Luca; Gul, Leila; Modos, Dezso; Madgwick, Matthew; Olbei, Marton; Bohar, Balazs; Valdeolivas, Alberto; Turei, Denes; Verstockt, Bram; Triana, Sergio; Alexandrov, Theodore; Saez-Rodriguez, Julio; Stanifer, Megan L.; Boulant, Steeve & Korcsmaros, Tamas
  
• Multivalent 9-O-Acetylated-sialic acid glycoclusters as potent inhibitors for SARS-CoV-2 infection. Nature Communications, 13(1).
  Petitjean, Simon J. L.; Chen, Wenzhang; Koehler, Melanie; Jimmidi, Ravikumar; Yang, Jinsung; Mohammed, Danahe; Juniku, Blinera; Stanifer, Megan L.; Boulant, Steeve; Vincent, Stéphane P. & Alsteens, David
  
• The FDA-Approved Drug Cobicistat Synergizes with Remdesivir To Inhibit SARS-CoV-2 Replication In Vitro and Decreases Viral Titers and Disease Progression in Syrian Hamsters. mBio, 13(2).
  Shytaj; Iart, Luca; Fares; Mohamed; Gallucci; Lara; Lucic; Bojana; Tolba; Mahmoud, M.; Zimmermann; Liv; Adler; Julia, M.; Xing; Na; Bushe; Judith; Gruber; Achim, D.; Ambiel; Ina; Taha, Ayoub; Ahmed; Cortese; Mirko; Neufeldt; Christopher, J.; Stolp; Bettina; Sobhy; Mohamed, Hossam; Fathy; Moustafa; Zhao; Min; Laketa; Vibor; ...; Lusic & Marina
  
• Type III and Not Type I Interferons Efficiently Prevent the Spread of Rotavirus in Human Intestinal Epithelial Cells. Journal of Virology, 96(17).
  Doldan, Patricio; Dai, Jin; Metz-Zumaran, Camila; Patton, John T.; Stanifer, Megan L. & Boulant, Steeve
  
• USP22 controls type III interferon signaling and SARS-CoV-2 infection through activation of STING. Cell Death & Disease, 13(8).
  Karlowitz, Rebekka; Stanifer, Megan L.; Roedig, Jens; Andrieux, Geoffroy; Bojkova, Denisa; Bechtel, Marco; Smith, Sonja; Kowald, Lisa; Schubert, Ralf; Boerries, Melanie; Cinatl, Jindrich; Boulant, Steeve & van Wijk Sjoerd, J. L.