Human TMEFF1 is a restriction factor for herpes simplex virus in the brain.
| Title: | Human TMEFF1 is a restriction factor for herpes simplex virus in the brain. |
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| Authors: | Chan YH; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA. chanyihao@me.com.; Liu Z; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Bastard P; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Khobrekar N; The Center for Stem Cell Biology & Developmental Biology Program, Sloan Kettering Institute for Cancer Research, New York, NY, USA.; Hutchison KM; Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.; Yamazaki Y; Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.; Fan Q; Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.; Matuozzo D; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Harschnitz O; The Center for Stem Cell Biology & Developmental Biology Program, Sloan Kettering Institute for Cancer Research, New York, NY, USA.; Human Technopole, Milan, Italy.; Kerrouche N; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Nakajima K; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Amin P; The Center for Stem Cell Biology & Developmental Biology Program, Sloan Kettering Institute for Cancer Research, New York, NY, USA.; Yatim A; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Rinchai D; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Chen J; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Zhang P; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Ciceri G; The Center for Stem Cell Biology & Developmental Biology Program, Sloan Kettering Institute for Cancer Research, New York, NY, USA.; Chen J; Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.; Dobbs K; Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.; Belkaya S; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Department of Molecular Biology and Genetics, Bilkent University, Ankara, Turkey.; Lee D; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Gervais A; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Aydın K; Department of Pediatric Neurology, Faculty of Medicine, Istanbul Medipol University, Istanbul, Turkey.; Kartal A; Child Neurology Department, Selcuk University, Konya, Turkey.; Hasek ML; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Zhao S; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Reino EG; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Lee YS; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Seeleuthner Y; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Chaldebas M; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Bailey R; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Vanhulle C; CHU Rouen Normandie, Rouen, France.; Lorenzo L; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Boucherit S; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Rozenberg F; Laboratory of Virology, Assistance Publique-Hôpitaux de Paris (AP-HP), Cochin Hospital, Paris, France.; Marr N; Research Branch, Sidra Medicine, Doha, Qatar.; Mogensen TH; Department of Biomedicine, Aarhus University, Aarhus, Denmark.; Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark.; Center for Immunology of Viral Infections, Aarhus University, Aarhus, Denmark.; Aubart M; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Pediatric Neurology Department, Necker Hospital for Sick Children, Paris-City University, Paris, France.; Cobat A; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Dulac O; Department of Pediatric Neurology, Necker Hospital for Sick Children, AP-HP, Paris, France.; Emiroglu M; Department of Pediatric Infectious Diseases, Faculty of Medicine, Selcuk University, Konya, Turkey.; Paludan SR; Department of Biomedicine, Aarhus University, Aarhus, Denmark.; Center for Immunology of Viral Infections, Aarhus University, Aarhus, Denmark.; Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Göteborg, Sweden.; Abel L; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.; Paris Cité University, Imagine Institute, Paris, France.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.; Notarangelo L; Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.; Longnecker R; Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.; Smith G; Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.; Studer L; The Center for Stem Cell Biology & Developmental Biology Program, Sloan Kettering Institute for Cancer Research, New York, NY, USA.; Casanova JL; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA. casanova@rockefeller.edu.; Paris Cité University, Imagine Institute, Paris, France. casanova@rockefeller.edu.; Pediatric Hematology-Immunology and Rheumatology Unit, Necker Hospital for Sick Children, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France. casanova@rockefeller.edu.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France. casanova@rockefeller.edu.; Howard Hughes Medical Institute, New York, NY, USA. casanova@rockefeller.edu.; Zhang SY; St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA. shzh289@rockefeller.edu.; Paris Cité University, Imagine Institute, Paris, France. shzh289@rockefeller.edu.; Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France. shzh289@rockefeller.edu. |
| Source: | Nature [Nature] 2024 Aug; Vol. 632 (8024), pp. 390-400. Date of Electronic Publication: 2024 Jul 24. |
| Publication Type: | Case Reports; Journal Article; Research Support, N.I.H., Extramural |
| Language: | English |
| Journal Info: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE |
| Imprint Name(s): | Publication: Basingstoke : Nature Publishing Group; Original Publication: London, Macmillan Journals ltd. |
| MeSH Terms: | Brain*/cytology ; Brain*/metabolism ; Brain*/virology ; Encephalitis, Herpes Simplex*/virology ; Encephalitis, Herpes Simplex*/metabolism ; Herpesvirus 1, Human*/pathogenicity ; Herpesvirus 1, Human*/physiology ; Membrane Proteins*/deficiency ; Membrane Proteins*/genetics ; Membrane Proteins*/metabolism ; Virus Internalization*; Interferon Type I/metabolism ; Interferon Type I/immunology ; Nectins/genetics ; Nectins/metabolism ; Neurons/cytology ; Neurons/metabolism ; Neurons/virology ; Pluripotent Stem Cells/cytology ; Animals ; Female ; Humans ; Male ; Homozygote ; Virus Replication ; Child, Preschool ; Young Adult ; Pedigree ; Neoplasm Proteins |
| Abstract: | Most cases of herpes simplex virus 1 (HSV-1) encephalitis (HSE) remain unexplained1,2. Here, we report on two unrelated people who had HSE as children and are homozygous for rare deleterious variants of TMEFF1, which encodes a cell membrane protein that is preferentially expressed by brain cortical neurons. TMEFF1 interacts with the cell-surface HSV-1 receptor NECTIN-1, impairing HSV-1 glycoprotein D- and NECTIN-1-mediated fusion of the virus and the cell membrane, blocking viral entry. Genetic TMEFF1 deficiency allows HSV-1 to rapidly enter cortical neurons that are either patient specific or derived from CRISPR-Cas9-engineered human pluripotent stem cells, thereby enhancing HSV-1 translocation to the nucleus and subsequent replication. This cellular phenotype can be rescued by pretreatment with type I interferon (IFN) or the expression of exogenous wild-type TMEFF1. Moreover, ectopic expression of full-length TMEFF1 or its amino-terminal extracellular domain, but not its carboxy-terminal intracellular domain, impairs HSV-1 entry into NECTIN-1-expressing cells other than neurons, increasing their resistance to HSV-1 infection. Human TMEFF1 is therefore a host restriction factor for HSV-1 entry into cortical neurons. Its constitutively high abundance in cortical neurons protects these cells from HSV-1 infection, whereas inherited TMEFF1 deficiency renders them susceptible to this virus and can therefore underlie HSE.; (© 2024. The Author(s).) |
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| Grant Information: | P30 CA008748 United States CA NCI NIH HHS; R01 AI088364 United States AI NIAID NIH HHS; R01 NS072381 United States NS NINDS NIH HHS; UL1 TR001866 United States TR NCATS NIH HHS |
| Substance Nomenclature: | 0 (Interferon Type I); 0 (Membrane Proteins); 0 (Nectins); 0 (NECTIN1 protein, human); 0 (TMEFF1 protein, human); 0 (Neoplasm Proteins) |
| Entry Date(s): | Date Created: 20240724 Date Completed: 20240807 Latest Revision: 20260409 |
| Update Code: | 20260409 |
| PubMed Central ID: | PMC11306101 |
| DOI: | 10.1038/s41586-024-07745-x |
| PMID: | 39048830 |
| Database: | MEDLINE |
Case Reports; Journal Article; Research Support, N.I.H., Extramural