Mutating novel interaction sites in NRP1 reduces SARS-CoV-2 spike protein internalization

Pal, Debjani; De, Kuntal; Yates, Timothy B.; Kolape, Jaydeep; Muchero, Wellington

doi:10.1016/j.isci.2023.106274

Title: Mutating novel interaction sites in NRP1 reduces SARS-CoV-2 spike protein internalization

Journal Article · Sat Apr 01 00:00:00 EDT 2023 · iScience

DOI:https://doi.org/10.1016/j.isci.2023.106274· OSTI ID:1958900

; De, Kuntal; Yates, Timothy B.; Kolape, Jaydeep; Muchero, Wellington

The global pandemic of coronavirus disease 2019 caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus has become a severe global health problem because of its rapid spread. Both Ace2 and NRP1 provide initial viral binding sites for SARS-CoV-2. Here, we show that cysteine residues located in the vestigial plasminogen-apple-nematode (PAN) domain of NRP1 are necessary for SARS-CoV-2 spike protein internalization. Mutating novel cysteine residues in the PAN altered NRP1 stability and downstream activation of extracellular signal-regulated kinase (ERK) signaling pathway and impaired its interaction with the spike protein. This resulted in a significant reduction in spike protein abundance in Vero-E6 cells for the original, alpha, and delta SARS-CoV-2 variants even in the presence of the Ace2. Moreover, mutating these cysteine residues in NRP1 significantly lowered its association with Plexin-A1. As the spike protein is a critical component for targeted therapy, our biochemical study may represent a distinct mechanism to develop a path for future therapeutic discovery.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; 3130F004

OSTI ID:: 1958900

Alternate ID(s):: OSTI ID: 1993703

Journal Information:: iScience, Journal Name: iScience Vol. 26 Journal Issue: 4; ISSN 2589-0042

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (76)

Neuropilin 1 is an entry factor that promotes EBV infection of nasopharyngeal epithelial cells Wang, Hong-Bo; Zhang, Hua; Zhang, Jing-Ping Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7240	journal	February 2015
Antiviral drugs targeting endosomal membrane proteins inhibit distant animal and human pathogenic viruses Galindo, I.; Garaigorta, U.; Lasala, F. Antiviral Research, Vol. 186 https://doi.org/10.1016/j.antiviral.2020.104990	journal	February 2021
Virus-receptor interactions of SARS-CoV-2 spikereceptor-binding domain and human neuropilin-1 b1 domain Alnomasy, Sultan F. Saudi Journal of Biological Sciences, Vol. 28, Issue 7 https://doi.org/10.1016/j.sjbs.2021.03.074	journal	July 2021
Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity Cantuti-Castelvetri, Ludovico; Ojha, Ravi; Pedro, Liliana D. Science, Vol. 370, Issue 6518 https://doi.org/10.1126/science.abd2985	journal	November 2020
IKKβ phosphorylation regulates RPS3 nuclear translocation and NF-κB function during infection with Escherichia coli strain O157:H7 Wan, Fengyi; Weaver, Amanda; Gao, Xiaofei Nature Immunology, Vol. 12, Issue 4 https://doi.org/10.1038/ni.2007	journal	March 2011
Ribosomal Protein S5 Interacts with the Internal Ribosomal Entry Site of Hepatitis C Virus Fukushi, Shuetsu; Okada, Masato; Stahl, Joachim Journal of Biological Chemistry, Vol. 276, Issue 24 https://doi.org/10.1074/jbc.C100206200	journal	June 2001
Structural and Functional Relation of Neuropilins Nakamura, Fumio; Goshima, Yoshio Neuropilin https://doi.org/10.1007/978-1-4615-0119-0_5	book	January 2002
Neuropilin-1 assists SARS-CoV-2 infection by stimulating the separation of Spike protein S1 and S2 Li, Zhen-lu; Buck, Matthias Biophysical Journal, Vol. 120, Issue 14 https://doi.org/10.1016/j.bpj.2021.05.026	journal	July 2021
Human DNA Virus Exploitation of the MAPK-ERK Cascade DuShane, Jeanne K.; Maginnis, Melissa S. International Journal of Molecular Sciences, Vol. 20, Issue 14 https://doi.org/10.3390/ijms20143427	journal	July 2019
Neuropilin Is a Semaphorin III Receptor Kolodkin, Alex L.; Levengood, Dorothy V.; Rowe, Erica G. Cell, Vol. 90, Issue 4 https://doi.org/10.1016/S0092-8674(00)80535-8	journal	August 1997
Comparative Proteomic Analysis of Anti-Cancer Mechanism by Periplocin Treatment in Lung Cancer Cells Lu, Zejun; Song, Qi; Yang, Jinliang Cellular Physiology and Biochemistry, Vol. 33, Issue 3 https://doi.org/10.1159/000358658	journal	January 2014
Neuropilin regulation of angiogenesis Lampropoulou, Anastasia; Ruhrberg, Christiana Biochemical Society Transactions, Vol. 42, Issue 6 https://doi.org/10.1042/BST20140244	journal	November 2014
Cell surface detection of vimentin, ACE2 and SARS-CoV-2 Spike proteins reveals selective colocalization at primary cilia Lalioti, Vasiliki; González-Sanz, Silvia; Lois-Bermejo, Irene Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-11248-y	journal	April 2022
Ribosomal Protein S3: A KH Domain Subunit in NF-κB Complexes that Mediates Selective Gene Regulation Wan, Fengyi; Anderson, D. Eric; Barnitz, Robert A. Cell, Vol. 131, Issue 5 https://doi.org/10.1016/j.cell.2007.10.009	journal	November 2007
A DERL3-associated defect in the degradation of SLC2A1 mediates the Warburg effect Lopez-Serra, Paula; Marcilla, Miguel; Villanueva, Alberto Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4608	journal	April 2014
Neuropilin-1 is a host factor for SARS-CoV-2 infection Daly, James L.; Simonetti, Boris; Klein, Katja Science, Vol. 370, Issue 6518 https://doi.org/10.1126/science.abd3072	journal	November 2020
The proteasome: Overview of structure and functions Tanaka, Keiji Proceedings of the Japan Academy, Series B, Vol. 85, Issue 1 https://doi.org/10.2183/pjab.85.12	journal	January 2009
β-Coronaviruses Use Lysosomes for Egress Instead of the Biosynthetic Secretory Pathway Ghosh, Sourish; Dellibovi-Ragheb, Teegan A.; Kerviel, Adeline Cell, Vol. 183, Issue 6 https://doi.org/10.1016/j.cell.2020.10.039	journal	December 2020
Immunopathology of Hyperinflammation in COVID-19 Gustine, Joshua N.; Jones, Dennis The American Journal of Pathology, Vol. 191, Issue 1 https://doi.org/10.1016/j.ajpath.2020.08.009	journal	January 2021
A Neuropilin-1 Antagonist Exerts Antitumor Immunity by Inhibiting the Suppressive Function of Intratumoral Regulatory T Cells Jung, Keunok; Kim, Jeong-Ah; Kim, Ye-Jin Cancer Immunology Research, Vol. 8, Issue 1 https://doi.org/10.1158/2326-6066.CIR-19-0143	journal	January 2020
The PAN module: the N-terminal domains of plasminogen and hepatocyte growth factor are homologous with the apple domains of the prekallikrein family and with a novel domain found in numerous nematode proteins Tordai, Hedvig; Bányai, László; Patthy, László FEBS Letters, Vol. 461, Issue 1-2 https://doi.org/10.1016/S0014-5793(99)01416-7	journal	November 1999
Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding Appleton, Brent A.; Wu, Ping; Maloney, Janice The EMBO Journal, Vol. 26, Issue 23 https://doi.org/10.1038/sj.emboj.7601906	journal	November 2007
Neuropilin-2, a Novel Member of the Neuropilin Family, Is a High Affinity Receptor for the Semaphorins Sema E and Sema IV but Not Sema III Chen, Hang; Chédotal, Alain; He, Zhigang Neuron, Vol. 19, Issue 3 https://doi.org/10.1016/S0896-6273(00)80371-2	journal	September 1997
NF-κB Pathway as a Potential Target for Treatment of Critical Stage COVID-19 Patients Kircheis, Ralf; Haasbach, Emanuel; Lueftenegger, Daniel Frontiers in Immunology, Vol. 11 https://doi.org/10.3389/fimmu.2020.598444	journal	December 2020
SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor Hoffmann, Markus; Kleine-Weber, Hannah; Schroeder, Simon Cell, Vol. 181, Issue 2 https://doi.org/10.1016/j.cell.2020.02.052	journal	April 2020
Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A Rohm, Beate; Ottemeyer, Angelika; Lohrum, Marion Mechanisms of Development, Vol. 93, Issue 1-2 https://doi.org/10.1016/S0925-4773(00)00269-0	journal	May 2000
Protein kinase LKB1 promotes RAB7-mediated neuropilin-1 degradation to inhibit angiogenesis Okon, Imoh S.; Coughlan, Kathleen A.; Zhang, Cheng Journal of Clinical Investigation, Vol. 124, Issue 10 https://doi.org/10.1172/JCI75371	journal	September 2014
Early Events in the Endoplasmic Reticulum Unfolded Protein Response Preissler, Steffen; Ron, David Cold Spring Harbor Perspectives in Biology, Vol. 11, Issue 4 https://doi.org/10.1101/cshperspect.a033894	journal	November 2018
MEK inhibitors reduce cellular expression of ACE2, pERK, pRb while stimulating NK-mediated cytotoxicity and attenuating inflammatory cytokines relevant to SARS-CoV-2 infection Zhou, Lanlan; Huntington, Kelsey; Zhang, Shengliang Oncotarget, Vol. 11, Issue 46 https://doi.org/10.18632/oncotarget.27799	journal	November 2020
C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration Teesalu, Tambet; Sugahara, Kazuki N.; Kotamraju, Venkata Ramana Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0908201106	journal	September 2009
PSMB7 is associated with anthracycline resistance and is a prognostic biomarker in breast cancer Munkácsy, G.; Abdul-Ghani, R.; Mihály, Z. British Journal of Cancer, Vol. 102, Issue 2 https://doi.org/10.1038/sj.bjc.6605478	journal	December 2009
VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding Soker, Shay; Miao, Hua-Quan; Nomi, Masashi Journal of Cellular Biochemistry, Vol. 85, Issue 2 https://doi.org/10.1002/jcb.10140	journal	January 2002
Maternal-larval population genetic traits in Stylophora pistillata, a hermaphroditic brooding coral species Douek, Jacob; Amar, Keren-Or; Rinkevich, Baruch Genetica, Vol. 139, Issue 11-12 https://doi.org/10.1007/s10709-012-9653-x	journal	December 2011
Role of the ERK1/2 Signaling Pathway in the Replication of Junín and Tacaribe Viruses Brunetti, Jesús; Foscaldi, Sabrina; Quintana, Verónica Viruses, Vol. 10, Issue 4 https://doi.org/10.3390/v10040199	journal	April 2018
Functional and Genomic Analyses Reveal an Essential Coordination between the Unfolded Protein Response and ER-Associated Degradation Travers, Kevin J.; Patil, Christopher K.; Wodicka, Lisa Cell, Vol. 101, Issue 3 https://doi.org/10.1016/S0092-8674(00)80835-1	journal	April 2000
Vascular endothelial growth factor regulates Stanniocalcin-1 expression via Neuropilin-1-dependent regulation of KDR and synergism with fibroblast growth Factor-2 Holmes, David I. R.; Zachary, Ian C. Cellular Signalling, Vol. 20, Issue 3 https://doi.org/10.1016/j.cellsig.2007.11.009	journal	March 2008
Inhibition of PlexA1-mediated brain tumor growth and tumor-associated angiogenesis using a transmembrane domain targeting peptide Jacob, Laurent; Sawma, Paul; Garnier, Norbert Oncotarget, Vol. 7, Issue 36 https://doi.org/10.18632/oncotarget.11072	journal	August 2016
Successful methods for transplanting fragments of Acropora formosa and Acropora hyacinthus Okubo, Nami; Taniguchi, Hiroki; Motokawa, Tatsuo Coral Reefs, Vol. 24, Issue 2 https://doi.org/10.1007/s00338-005-0496-0	journal	May 2005
Targeting Neuropilin-1 with Nanobodies Reduces Colorectal Carcinoma Development De Vlaeminck, Yannick; Bonelli, Stefano; Awad, Robin Maximilian Cancers, Vol. 12, Issue 12 https://doi.org/10.3390/cancers12123582	journal	November 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Molecular basis of the new COVID-19 target neuropilin-1 in complex with SARS-CoV-2 S1 C-end rule peptide and small-molecule antagonists Klaewkla, Methus; Charoenwongpaiboon, Thanapon; Mahalapbutr, Panupong Journal of Molecular Liquids, Vol. 335 https://doi.org/10.1016/j.molliq.2021.116537	journal	August 2021
Sox2 is associated with cancer stem-like properties in colorectal cancer Takeda, Koki; Mizushima, Tsunekazu; Yokoyama, Yuhki Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-36251-0	journal	December 2018
NF-κB c-Rel Dictates the Inflammatory Threshold by Acting as a Transcriptional Repressor de Jesús, Tristan James; Ramakrishnan, Parameswaran iScience, Vol. 23, Issue 3 https://doi.org/10.1016/j.isci.2020.100876	journal	March 2020
Neuropilin-1 Binds Vascular Endothelial Growth Factor 165, Placenta Growth Factor-2, and Heparin via Its b1b2 Domain Mamluk, Roni; Gechtman, Ze'ev; Kutcher, Matthew E. Journal of Biological Chemistry, Vol. 277, Issue 27 https://doi.org/10.1074/jbc.M200730200	journal	July 2002
Receptor complexes for each of the Class 3 Semaphorins Sharma, Anil; Verhaagen, Joost; Harvey, Alan R. Frontiers in Cellular Neuroscience, Vol. 6 https://doi.org/10.3389/fncel.2012.00028	journal	January 2012
The 20S proteasome processes NF-κB1 p105 into p50 in a translation-independent manner Moorthy, Anu K.; Savinova, Olga V.; Ho, Jessica Q. The EMBO Journal, Vol. 25, Issue 9 https://doi.org/10.1038/sj.emboj.7601081	journal	April 2006
RNA viruses and the mitogenic Raf/MEK/ERK signal transduction cascade Pleschka, Stephan bchm, Vol. 389, Issue 10 https://doi.org/10.1515/BC.2008.145	journal	August 2008
Characterization of the Interaction between Hantavirus Nucleocapsid Protein (N) and Ribosomal Protein S19 (RPS19) Cheng, Erdong; Haque, Absarul; Rimmer, Mary Ashley Journal of Biological Chemistry, Vol. 286, Issue 13 https://doi.org/10.1074/jbc.M110.210179	journal	April 2011
Coronavirus infection, ER stress, apoptosis and innate immunity Fung, To S.; Liu, Ding X. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00296	journal	June 2014
A phase I study of the human monoclonal anti-NRP1 antibody MNRP1685A in patients with advanced solid tumors Weekes, Colin D.; Beeram, Muralidhar; Tolcher, Anthony W. Investigational New Drugs, Vol. 32, Issue 4 https://doi.org/10.1007/s10637-014-0071-z	journal	March 2014
Dual Function of NRP1 in Axon Guidance and Subcellular Target Recognition in Cerebellum Telley, Ludovic; Cadilhac, Christelle; Cioni, Jean-Michel Neuron, Vol. 91, Issue 6 https://doi.org/10.1016/j.neuron.2016.08.015	journal	September 2016
The immunoproteasome and viral infection: a complex regulator of inflammation McCarthy, Mary K.; Weinberg, Jason B. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00021	journal	January 2015
KIF20A promotes the development of fibrosarcoma via PI3K-Akt signaling pathway Jin, Zheng; Tao, Shuang; Zhang, Chao Experimental Cell Research, Vol. 420, Issue 1 https://doi.org/10.1016/j.yexcr.2022.113322	journal	November 2022
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Rig-I regulates NF-κB activity through binding to Nf-κb1 3′-UTR mRNA Zhang, Hong-Xin; Liu, Zi-Xing; Sun, Yue-Ping Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1304432110	journal	April 2013
Neuropilin-1: A Key Protein to Consider in the Progression of Pediatric Brain Tumors Douyère, Manon; Chastagner, Pascal; Boura, Cédric Frontiers in Oncology, Vol. 11 https://doi.org/10.3389/fonc.2021.665634	journal	July 2021
Core cysteine residues in the Plasminogen-Apple-Nematode (PAN) domain are critical for HGF/c-MET signaling Pal, Debjani; De, Kuntal; Shanks, Carly M. Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03582-8	journal	July 2022
SARS-CoV-2 Infection-Induced Promoter Hypomethylation as an Epigenetic Modulator of Heat Shock Protein A1L (HSPA1L) Gene Muhammad, Jibran Sualeh; Saheb Sharif-Askari, Narjes; Cui, Zheng-Guo Frontiers in Genetics, Vol. 12 https://doi.org/10.3389/fgene.2021.622271	journal	February 2021
The role of TACC3 in mitotic spindle organization Ding, Zhi-Ming; Huang, Chun-Jie; Jiao, Xiao-Fei Cytoskeleton, Vol. 74, Issue 10 https://doi.org/10.1002/cm.21388	journal	August 2017
The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors Takagi, Shin; Hirata, Tatsumi; Agata, Kiyokazu Neuron, Vol. 7, Issue 2 https://doi.org/10.1016/0896-6273(91)90268-5	journal	August 1991
Plexin-Neuropilin-1 Complexes Form Functional Semaphorin-3A Receptors Takahashi, Takuya; Fournier, Alyson; Nakamura, Fumio Cell, Vol. 99, Issue 1 https://doi.org/10.1016/S0092-8674(00)80062-8	journal	October 1999
HMMER web server: 2015 update Finn, Robert D.; Clements, Jody; Arndt, William Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv397	journal	May 2015
Visna Virus-Induced Activation of MAPK Is Required for Virus Replication and Correlates with Virus-Induced Neuropathology Barber, Sheila A.; Bruett, Linda; Douglass, Brian R. Journal of Virology, Vol. 76, Issue 2 https://doi.org/10.1128/JVI.76.2.817-828.2002	journal	January 2002
Origin and the Early Evolution of the Phylum Mollusca Parkhaev, P. Yu. Paleontological Journal, Vol. 51, Issue 6 https://doi.org/10.1134/S003103011706003X	journal	November 2017
Characterization of peptide binding to the SARS-CoV-2 host factor neuropilin Jobe, Amie; Vijayan, Ranjit Heliyon, Vol. 7, Issue 10 https://doi.org/10.1016/j.heliyon.2021.e08251	journal	October 2021
The many faces of semaphorins: from development to pathology Roth, L.; Koncina, E.; Satkauskas, S. Cellular and Molecular Life Sciences, Vol. 66, Issue 4 https://doi.org/10.1007/s00018-008-8518-z	journal	October 2008
Signaling through the P38 and ERK pathways: a common link between HIV replication and the immune response Furler, Robert L.; Uittenbogaart, Christel H. Immunologic Research, Vol. 48, Issue 1-3 https://doi.org/10.1007/s12026-010-8170-1	journal	August 2010
ERO1-β, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis Zito, Ester; Chin, King-Tung; Blais, Jaime Journal of Cell Biology, Vol. 188, Issue 6 https://doi.org/10.1083/jcb.200911086	journal	March 2010
An adhesive domain detected in functionally diverse receptors Beckmann, Georg; Bork, Peer Trends in Biochemical Sciences, Vol. 18, Issue 2 https://doi.org/10.1016/0968-0004(93)90049-S	journal	February 1993
Neuropilins: expression and roles in the epithelium Wild, Jonathan R. L.; Staton, Carolyn A.; Chapple, Keith International Journal of Experimental Pathology, Vol. 93, Issue 2 https://doi.org/10.1111/j.1365-2613.2012.00810.x	journal	March 2012
Neuropilins in the Context of Tumor Vasculature Niland, Stephan; Eble, Johannes A. International Journal of Molecular Sciences, Vol. 20, Issue 3 https://doi.org/10.3390/ijms20030639	journal	February 2019
Molluscs Haszprunar, Gerhard; Wanninger, Andreas Current Biology, Vol. 22, Issue 13 https://doi.org/10.1016/j.cub.2012.05.039	journal	July 2012
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Effect of C-Terminal Sequence on Competitive Semaphorin Binding to Neuropilin-1 Parker, Matthew W.; Linkugel, Andrew D.; Vander Kooi, Craig W. Journal of Molecular Biology, Vol. 425, Issue 22 https://doi.org/10.1016/j.jmb.2013.07.017	journal	November 2013
RPLP1 and RPLP2 Are Essential Flavivirus Host Factors That Promote Early Viral Protein Accumulation Campos, Rafael K.; Wong, Benjamin; Xie, Xuping Journal of Virology, Vol. 91, Issue 4 https://doi.org/10.1128/JVI.01706-16	journal	February 2017
Induction of Herpud1 expression by ER stress is regulated by Nrf1 Ho, Daniel V.; Chan, Jefferson Y. FEBS Letters, Vol. 589, Issue 5 https://doi.org/10.1016/j.febslet.2015.01.026	journal	January 2015

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