Human OTULIN haploinsufficiency impairs cell-intrinsic immunity to staphylococcal α-toxin-Reference-Cited by-同舟云学术

Human OTULIN haploinsufficiency impairs cell-intrinsic immunity to staphylococcal α-toxin

Published:2022-06-17 Issue:6599 Volume:376 Page:
ISSN:0036-8075
Container-title:Science
language:en
Short-container-title:Science

Author:

Spaan András N.¹²^ORCID,Neehus Anna-Lena³⁴⁵^ORCID,Laplantine Emmanuel⁶⁷^ORCID,Staels Frederik⁸^ORCID,Ogishi Masato¹^ORCID,Seeleuthner Yoann³⁴,Rapaport Franck¹^ORCID,Lacey Keenan A.⁹^ORCID,Van Nieuwenhove Erika⁸¹⁰^ORCID,Chrabieh Maya³⁴,Hum David¹^ORCID,Migaud Mélanie³⁴^ORCID,Izmiryan Araksya⁴¹¹^ORCID,Lorenzo Lazaro³⁴^ORCID,Kochetkov Tatiana¹,Heesterbeek Dani A. C.²^ORCID,Bardoel Bart W.²^ORCID,DuMont Ashley L.⁹^ORCID,Dobbs Kerry¹²^ORCID,Chardonnet Solenne¹³^ORCID,Heissel Søren¹⁴,Baslan Timour¹⁵,Zhang Peng¹^ORCID,Yang Rui¹^ORCID,Bogunovic Dusan¹⁶,Wunderink Herman F.²^ORCID,Haas Pieter-Jan A.²,Molina Henrik¹⁴^ORCID,Van Buggenhout Griet¹⁷¹⁸,Lyonnet Stanislas⁴¹⁹,Notarangelo Luigi D.¹²^ORCID,Seppänen Mikko R. J.²⁰^ORCID,Weil Robert⁶^ORCID,Seminario Gisela²¹,Gomez-Tello Héctor²²^ORCID,Wouters Carine⁸²³^ORCID,Mesdaghi Mehrnaz²⁴^ORCID,Shahrooei Mohammad²⁵²⁶,Bossuyt Xavier²⁵,Sag Erdal²⁷^ORCID,Topaloglu Rezan²⁸^ORCID,Ozen Seza²⁷^ORCID,Leavis Helen L.²⁹^ORCID,van Eijk Maarten M. J.³⁰^ORCID,Bezrodnik Liliana²¹,Blancas Galicia Lizbeth³¹^ORCID,Hovnanian Alain⁴¹¹³²^ORCID,Nassif Aude³³^ORCID,Bader-Meunier Brigitte⁴³⁴³⁵^ORCID,Neven Bénédicte⁴³⁴³⁵,Meyts Isabelle³⁶³⁷^ORCID,Schrijvers Rik³⁸^ORCID,Puel Anne¹³⁴^ORCID,Bustamante Jacinta¹³⁴³⁹^ORCID,Aksentijevich Ivona⁴⁰^ORCID,Kastner Daniel L.⁴⁰^ORCID,Torres Victor J.⁹^ORCID,Humblet-Baron Stéphanie⁸^ORCID,Liston Adrian⁸⁴¹⁴²^ORCID,Abel Laurent¹³⁴^ORCID,Boisson Bertrand¹³⁴^ORCID,Casanova Jean-Laurent¹³⁴⁴³⁴⁴^ORCID

Affiliation:

1. St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY 10065, USA.

2. Department of Medical Microbiology, University Medical Center Utrecht, Utrecht University, 3584 CX Utrecht, Netherlands.

3. Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, 75015 Paris, France.

4. Imagine Institute, Paris Cité University, 75015 Paris, France.

5. Institute of Experimental Hematology, REBIRTH Research Center for Translational and Regenerative Medicine, Hannover Medical School, 30625 Hannover, Germany.

6. Centre d’Immunologie et des Maladies Infectieuses, INSERM U1135, CNRS ERL8255, Sorbonne University, 75724 Paris, France.

7. Institut de Recherche St. Louis, Hôpital St. Louis, INSERM U944, CNRS U7212, Paris Cité University, 75010 Paris, France.

8. Laboratory for Adaptive Immunology, Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium.

9. Department of Microbiology, New York University Grossman School of Medicine, New York, NY 10016, USA.

10. Department of Pediatric Rheumatology and Immunology, Wilhelmina Children’s Hospital, University Medical Center Utrecht, Utrecht University, 3584 CX Utrecht, Netherlands.

11. Laboratory of Genetic Skin Diseases, INSERM U1163, 75015 Paris, France.

12. Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD 20852, USA.

13. Plateforme Post-génomique de la Pitié-Salpêtrière, P3S, UMS Production et Analyse de données en Sciences de la vie et en Santé, PASS, INSERM, Sorbonne University, 75013 Paris, France.

14. Proteomics Resource Center, The Rockefeller University, New York, NY 10065, USA.

15. Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.

16. Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.

17. Department of Human Genetics, KU Leuven, 3000 Leuven, Belgium.

18. Center for Human Genetics, University Hospitals Leuven, 3000 Leuven, Belgium.

19. Laboratory Embryology and Genetics of Malformations, INSERM U1163, Necker Hospital for Sick Children, 75015 Paris, France.

20. Rare Disease and Pediatric Research Centers, Children and Adolescents, University of Helsinki and HUS Helsinki University Hospital, 00260 Helsinki, Finland.

21. Center for Clinical Immunology, Immunology Group Children’s Hospital Ricardo Gutiérrez, C1425EFD Buenos Aires, Argentina.

22. Immunology Department, Poblano Children’s Hospital, 72190 Puebla, Mexico.

23. Department of Pediatrics, University Hospitals Leuven, 3000 Leuven, Belgium.

24. Department of Allergy and Clinical Immunology, Mofid Children’s Hospital, Shahid Beheshti University of Medical Sciences, 15468-155514 Tehran, Iran.

25. Clinical and Diagnostic Immunology, Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium.

26. Specialized Immunology Laboratory of Dr. Shahrooei, Sina Medical Complex, 15468-155514 Ahvaz, Iran.

27. Department of Pediatric Rheumatology, Hacettepe University, 06230 Ankara, Turkey.

28. Department of Pediatric Nephrology, Hacettepe University School of Medicine, Hacettepe University, 06230 Ankara, Turkey.

29. Department of Rheumatology and Clinical Immunology, University Medical Center Utrecht, Utrecht University, 3584 CX Utrecht, Netherlands.

30. Department of Intensive Care Medicine, University Medical Center Utrecht, Utrecht University, 3584 CX Utrecht, Netherlands.

31. Immune Deficiencies Laboratory National Institute of Pediatrics, 04530 Mexico City, Mexico.

32. Department of Genetics, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France.

33. Centre Médical, Institut Pasteur, 75724 Paris, France.

34. Pediatric Immunology, Hematology and Rheumatology Unit, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France.

35. Laboratory of Immunogenetics of Pediatric Autoimmunity, INSERM U1163, Necker Hospital for Sick Children, 75015 Paris, France.

36. Laboratory of Inborn Errors of Immunity, Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium.

37. Department of Pediatrics, Jeffrey Modell Diagnostic and Research Network Center, University Hospitals Leuven, 3000 Leuven, Belgium.

38. Allergy and Clinical Immunology Research Group, Department of Microbiology, Immunology and Transplantation, KU Leuven, 3000 Leuven, Belgium.

39. Study Center for Primary Immunodeficiencies, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France.

40. Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, MD 20892, USA.

41. VIB Center for Brain and Disease Research, Leuven 3000, Belgium.

42. Immunology Programme, Babraham Institute, Babraham Research Campus, Cambridge CB22 3AT, UK.

43. Department of Pediatrics, Necker Hospital for Sick Children, AP-HP, 75015 Paris, France.

44. Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA.

Abstract

The molecular basis of interindividual clinical variability upon infection withStaphylococcus aureusis unclear. We describe patients with haploinsufficiency for the linear deubiquitinase OTULIN, encoded by a gene on chromosome 5p. Patients suffer from episodes of life-threatening necrosis, typically triggered byS. aureusinfection. The disorder is phenocopied in patients with the 5p− (Cri-du-Chat) chromosomal deletion syndrome. OTULIN haploinsufficiency causes an accumulation of linear ubiquitin in dermal fibroblasts, but tumor necrosis factor receptor–mediated nuclear factor κB signaling remains intact. Blood leukocyte subsets are unaffected. The OTULIN-dependent accumulation of caveolin-1 in dermal fibroblasts, but not leukocytes, facilitates the cytotoxic damage inflicted by the staphylococcal virulence factor α-toxin. Naturally elicited antibodies against α-toxin contribute to incomplete clinical penetrance. Human OTULIN haploinsufficiency underlies life-threatening staphylococcal disease by disrupting cell-intrinsic immunity to α-toxin in nonleukocytic cells.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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