본문 바로가기
KERD
논문KCI 등재

SARS-CoV-2 Infection Induces HMGB1 Secretion Through Post-Translational Modification and PANoptosis

0

조회

0

다운로드

0

인용

0

참고문헌

키워드

초록

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection induces excessive pro-inflammatory cytokine release and cell death, leading to organ damage and mortality. High-mobility group box 1 (HMGB1) is one of the damage-associated molecular patterns that can be secreted by pro-inflammatory stimuli, including viral infections, and its excessive secretion levels are related to a variety of inflammatory diseases. Here, the aim of the study was to show that SARS-CoV-2 infection induced HMGB1 secretion via active and passive release. Active HMGB1 secretion was mediated by post-translational modifications, such as acetylation, phosphorylation, and oxidation in HEK293E/ACE2-C-GFP and Calu-3 cells during SARS-CoV-2 infection. Passive release of HMGB1 has been linked to various types of cell death; however, we demonstrated for the first time that PANoptosis, which integrates other cell death pathways, including pyroptosis, apoptosis, and necroptosis, is related to passive HMGB1 release during SARS-CoV-2 infection. In addition, cytoplasmic translocation and extracellular secretion or release of HMGB1 were confirmed via immunohistochemistry and immunofluorescence in the lung tissues of humans and angiotensin-converting enzyme 2-overexpressing mice infected with SARS-CoV-2.

Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection induces excessive pro-inflammatory cytokine release and cell death, leading to organ damage and mortality. High-mobility group box 1 (HMGB1) is one of the damage-associated molecular patterns that can be secreted by pro-inflammatory stimuli, including viral infections, and its excessive secretion levels are related to a variety of inflammatory diseases. Here, the aim of the study was to show that SARS-CoV-2 infection induced HMGB1 secretion via active and passive release. Active HMGB1 secretion was mediated by post-translational modifications, such as acetylation, phosphorylation, and oxidation in HEK293E/ACE2-C-GFP and Calu-3 cells during SARS-CoV-2 infection. Passive release of HMGB1 has been linked to various types of cell death; however, we demonstrated for the first time that PANoptosis, which integrates other cell death pathways, including pyroptosis, apoptosis, and necroptosis, is related to passive HMGB1 release during SARS-CoV-2 infection. In addition, cytoplasmic translocation and extracellular secretion or release of HMGB1 were confirmed via immunohistochemistry and immunofluorescence in the lung tissues of humans and angiotensin-converting enzyme 2-overexpressing mice infected with SARS-CoV-2.

참고문헌 (63)

  1. Kahn JS, "History and recent advances in coronavirus discovery", Pediatr Infect Dis J, 24, pp.S223~S227 (2005)
  2. Cameroni E, "Broadly neutralizing antibodies overcome SARS-CoV-2 omicron antigenic shift", Nature, 602, pp.664~670 (2022)
  3. 최준용, "SARS-CoV-2 Variants of Concern", Yonsei Medical Journal, 62(11), pp.961~968 (2021), 연세대학교의과대학[DOI]
  4. Dong Hoon Shin, "SARS-CoV-2 Omicron Variant of Concern: Everything You Wanted to Know about Omicron but Were Afraid to Ask", Yonsei Medical Journal, 63(11), pp.977~983 (2022), 연세대학교의과대학[DOI]
  5. Yan R, "Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2", Science, 367, pp.1444~1448 (2020)
  6. Lu R, "Genomic characterisation and epidemiology of 2019 novel coronavirus : implications for virus origins and receptor binding", Lancet, 395, pp.565~574 (2020)
  7. Kim Sinae, "SARS-CoV-2 Omicron Mutation Is Faster than the Chase: Multiple Mutations on Spike", ACE2 Interaction Residues, 2021, pp.21(6), 1~8[DOI]
  8. Hoffmann M, "SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor", Cell, 181, pp.271~280 (2020)
  9. Bayati A, "SARS-CoV-2 infects cells after viral entry via clathrin-mediated endocytosis", J Biol Chem, 296, pp.100306~ (2021)
  10. 강연우, "Understanding the Host Innate Immune Responses against SARS-CoV-2 Infection and COVID-19 Pathogenesis", Immune Network, 21(1), pp.1~16 (2021), 대한면역학회[DOI]
  11. Ren Y, "The ORF3a protein of SARS-CoV-2 induces apoptosis in cells", Cell Mol Immunol, 17, pp.881~883 (2020)
  12. Li S, "SARS-CoV-2 triggers inflammatory responses and cell death through caspase-8 activation", Signal Transduct Target Ther, 5, pp.235~ (2020)
  13. Karki R, "Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes", Cell, 184, pp.149~168 (2021)
  14. Ivanisenko NV, "The role of death domain proteins in host response upon SARS-CoV-2 infection : modulation of programmed cell death and translational applications", Cell Death Dis, 6, pp.101~ (2020)
  15. Kuriakose T, "ZBP1", DAI is an innate sensor of influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways, 2016, pp.1, ~
  16. Lee S, "AIM2 forms a complex with pyrin and ZBP1 to drive PANoptosis and host defence", Nature, 597, pp.415~419 (2021)
  17. Karki R, "ZBP1-dependent inflammatory cell death, PANoptosis, and cytokine storm disrupt IFN therapeutic efficacy during coronavirus infection", Sci Immunol, pp.7~ (2022)
  18. Del Valle DM, "An inflammatory cytokine signature predicts COVID-19 severity and survival", Nat Med, 26, pp.1636~1643 (2020)
  19. Karki R, "ZBP1-dependent inflammatory cell death, PANoptosis, and cytokine storm disrupt IFN therapeutic efficacy during coronavirus infection", Sci Immunol, 7 (2022)
  20. Wang H, "HMGB1 as a late mediator of lethal systemic inflammation", Am J Respir Crit Care Med, 164, pp.1768~1773 (2001)
  21. Chen R, "HMGB1 as a potential biomarker and therapeutic target for severe COVID-19", Heliyon(Lond), 6, pp.e05672~ (2020)
  22. Bustin M, "High-mobility-group chromosomal proteins : architectural components that facilitate chromatin function", Prog Nucleic Acid Res Mol Biol, 54, pp.35~100 (1996)
  23. Bianchi ME, "Specific recognition of cruciform DNA by nuclear protein HMG1", Science, 243, pp.1056~1059 (1989)
  24. Lotze MT, "High-mobility group box 1 protein(HMGB1) : nuclear weapon in the immune arsenal", Nat Rev Immunol, 5, pp.331~342 (2005)
  25. Watanabe T, "The role of HMGB-1 on the development of necrosis during hepatic ischemia and hepatic ischemia", reperfusion injury in mice, 2005, pp.124, 59~66
  26. Yanai H, "HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses", Nature, 462, pp.99~103 (2009)
  27. Scaffidi P, "Release of chromatin protein HMGB1 by necrotic cells triggers inflammation", Nature, 418, pp.191~195 (2002)
  28. Kwak MS, "Immunological significance of HMGB1 post-translational modification and redox biology", Front Immunol, 11, pp.1189~ (2020)
  29. Bonaldi T, "Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion", EMBO J, 22, pp.5551~5560 (2003)
  30. Youn JH, "Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion", J Immunol, 177, pp.7889~7897 (2006)
  31. Kim YH, "N-linked glycosylation plays a crucial role in the secretion of HMGB1", J Cell Sci, 129, pp.29~38 (2016)
  32. Ito I, "Post-translational methylation of high mobility group box 1(HMGB1)causes its cytoplasmic localization in neutrophils", J Biol Chem, 282, pp.16336~16344 (2007)
  33. Kwak MS, "Peroxiredoxin-mediated disulfide bond formation is required for nucleocytoplasmic translocation and secretion of HMGB1 in response to inflammatory stimuli", Redox Biol, 24, pp.101203~ (2019)
  34. Davis K, "Poly(ADP-ribosyl)ation of high mobility group box 1(HMGB1)protein enhances inhibition of efferocytosis", Mol Med, 18, pp.359~369 (2012)
  35. Schiraldi M, "HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4", J Exp Med, 209, pp.551~563 (2012)
  36. Yang H, "A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release", Proc Natl Acad Sci U S A, 107, pp.11942~11947 (2010)
  37. Kazama H, "Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein", Immunity, 29, pp.21~32 (2008)
  38. Lu B, "Novel role of PKR in inflammasome activation and HMGB1 release", Nature, 488, pp.670~674 (2012)
  39. Qin S, "Role of HMGB1 in apoptosis-mediated sepsis lethality", J Exp Med, 203, pp.1637~1642 (2006)
  40. Quarato G, "Sequential engagement of distinct MLKL phosphatidylinositol-binding sites executes necroptosis", Mol Cell, 61, pp.589~601 (2016)
  41. Youn JH, "High mobility group box 1 protein binding to lipopolysaccharide facilitates transfer of lipopolysaccharide to CD14 and enhances lipopolysaccharide-mediated TNF-α production in human monocytes", J Immunol, 180, pp.5067~5074 (2008)
  42. Youn JH, "Identification of lipopolysaccharide-binding peptide regions within HMGB1 and their effects on subclinical endotoxemia in a mouse model", Eur J Immunol, 41, pp.2753~2762 (2011)
  43. Kwak MS, "HMGB1 binds to lipoteichoic acid and enhances TNF-α and IL-6 production through HMGB1-mediated transfer of lipoteichoic acid to CD14 and TLR2", J Innate Immun, 7, pp.405~416 (2015)
  44. Ivanov S, "A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA", Blood, 110, pp.1970~1981 (2007)
  45. Andersson U, "HMGB1 is a therapeutic target for sterile inflammation and infection", Annu Rev Immunol, 29, pp.139~162 (2011)
  46. Andersson U, "Extracellular HMGB1 as a therapeutic target in inflammatory diseases", Expert Opin Ther Targets, 22, pp.263~277 (2018)
  47. Xue J, "HMGB1 as a therapeutic target in disease", J Cell Physiol, 236, pp.3406~3419 (2021)
  48. Chen J, "Cell death triggers induce MLKL cleavage in multiple myeloma cells, which may promote cell death", Front Oncol, 12, pp.907036~ (2022)
  49. Kim YH, "Secretory autophagy machinery and vesicular trafficking are involved in HMGB1 secretion", Autophagy, 17, pp.2345~2362 (2021)
  50. Kim DM, "Enhanced eosinophil-mediated inflammation associated with antibody and complement-dependent pneumonic insults in critical COVID-19", Cell Reports, 37, pp.109798~ (2021)
  51. Cao DW, "The lncRNA Malat1 functions as a ceRNA to contribute to berberine-mediated inhibition of HMGB1 by sponging miR-181c-5p in poststroke inflammation", Acta Pharmacol Sin, 41, pp.22~33 (2020)
  52. Qu Y, "Newcastle disease virus infection triggers HMGB1 release to promote the inflammatory response", Virology, 525, pp.19~31 (2018)
  53. 이신애, "The Role of High Mobility Group Box 1 in Innate Immunity", Yonsei Medical Journal, 55(5), pp.1165~1176 (2014), 연세대학교의과대학[DOI]
  54. Kwak MS, "Reactive oxygen species induce Cys106-mediated anti-parallel HMGB1 dimerization that protects against DNA damage", Redox Biol, 40, pp.101858~ (2021)
  55. Wei J, "Genome-wide CRISPR screens reveal host factors critical for SARS-CoV-2 infection", Cell, 184, pp.76~91 (2021)
  56. Stasi A, "SARS-CoV-2 and viral sepsis : immune dysfunction and implications in kidney failure", J Clin Med, 9, pp.4057~ (2020)
  57. Chen YM, "Blood molecular markers associated with COVID-19 immunopathology and multi-organ damage", EMBO J, 39, pp.e105896~ (2020)
  58. Wiersinga WJ, "Pathophysiology, transmission, diagnosis, and treatment of coronavirus disease 2019(COVID-19) : a review", JAMA, 324, pp.782~793 (2020)
  59. Wu M, "Severe COVID-19-associated sepsis is different from classical sepsis induced by pulmonary infection with carbapenem-resistant klebsiella pneumonia(CrKP)", Chin J Traumatol, 25, pp.17~24 (2022)
  60. Wang H, "HMG-1 as a late mediator of endotoxin lethality in mice", Science, 285, pp.248~251 (1999)
  61. Kim SY, "High-mobility group box 1-induced complement activation causes sterile inflammation", Front Immunol, 9, pp.705~ (2018)
  62. Berthelot F, "The effect of HMGB1, a damage-associated molecular pattern molecule, on polymorphonuclear neutrophil migration depends on its concentration", J Innate Immun, 4, pp.41~58 (2012)
  63. Zheng J, "COVID-19 treatments and pathogenesis including anosmia in K18-hACE2 mice", Nature, 589, pp.603~607 (2021)

관련 논문AI추천

이 간행물의 다른 논문 (6건)