Skip to main content

Advertisement

SpringerLink
Log in

Pyroptosis in microbial infectious diseases

  • Review
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Pyroptosis is a gasdermins-mediated programmed cell death that plays an essential role in immune regulation, and its role in autoimmune disease and cancer has been studied extensively. Increasing evidence shows that various microbial infections can lead to pyroptosis, associated with the occurrence and development of microbial infectious diseases. This study reviews the recent advances in pyroptosis in microbial infection, including bacterial, viral, and fungal infections. We also explore potential therapeutic strategies for treating microbial infection-related diseases by targeting pyroptosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  1. Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358(6382):167–169. https://doi.org/10.1038/358167a0

    Article  PubMed  Google Scholar 

  2. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96(5):2396–2401. https://doi.org/10.1073/pnas.96.5.2396

    Article  PubMed  PubMed Central  Google Scholar 

  3. Cookson BT, Brennan MA (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9(3):113–114. https://doi.org/10.1016/s0966-842x(00)01936-3

    Article  PubMed  Google Scholar 

  4. Ruan J, Wang S, Wang J (2020) Mechanism and regulation of pyroptosis-mediated in cancer cell death. Chem Biol Interact 323(e133727):109052. https://doi.org/10.1016/j.cbi.2020.109052

    Article  PubMed  Google Scholar 

  5. Sangiuliano B, Pérez NM, Moreira DF, Belizário JE (2014) Cell death-associated molecular-pattern molecules: inflammatory signaling and control. Mediators Inflamm 2014:821043. https://doi.org/10.1155/2014/821043

    Article  PubMed  PubMed Central  Google Scholar 

  6. Zou J, Zheng Y, Huang Y, Tang D, Kang R, Chen R (2021) The versatile Gasdermin Family: their function and roles in Diseases. Front Immunol 12:751533. https://doi.org/10.3389/fimmu.2021.751533

    Article  PubMed  PubMed Central  Google Scholar 

  7. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526(7575):660–665. https://doi.org/10.1038/nature15514

    Article  PubMed  Google Scholar 

  8. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, Sun H, Wang DC, Shao F (2016) Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535(7610):111–116. https://doi.org/10.1038/nature18590

    Article  PubMed  Google Scholar 

  9. Man SM, Karki R, Kanneganti TD (2017) Molecular mechanisms and functions of pyroptosis, inflammatory caspases and inflammasomes in infectious Diseases. Immunol Rev 277(1):61–75. https://doi.org/10.1111/imr.12534

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sarhan J, Liu BC, Muendlein HI, Li P, Nilson R, Tang AY, Rongvaux A, Bunnell SC, Shao F, Green DR, Poltorak A (2018) Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia Infection. Proc Natl Acad Sci U S A 115(46):E10888–E10897. https://doi.org/10.1073/pnas.1809548115

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wang Y, Gao W, Shi X, Ding J, Liu W, He H, Wang K, Shao F (2017) Chemotherapy Drugs induce pyroptosis through caspase-3 cleavage of a gasdermin. Nature 547(7661):99–103. https://doi.org/10.1038/nature22393

    Article  PubMed  Google Scholar 

  12. Rogers C, Fernandes-Alnemri T, Mayes L, Alnemri D, Cingolani G, Alnemri ES (2017) Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death. Nat Commun 8:14128. https://doi.org/10.1038/ncomms14128

    Article  PubMed  PubMed Central  Google Scholar 

  13. Jiang S, Gu H, Zhao Y, Sun L (2019) Teleost Gasdermin E is cleaved by Caspase 1, 3, and 7 and induces pyroptosis. J Immunol 203(5):1369–1382. https://doi.org/10.4049/jimmunol.1900383

    Article  PubMed  Google Scholar 

  14. Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157(5):1013–1022. https://doi.org/10.1016/j.cell.2014.04.007

    Article  PubMed  Google Scholar 

  15. Wang W, Zhang T (2018) Caspase-1-Mediated pyroptosis of the predominance for driving CD4[Formula: see text] T cells death: a nonlocal spatial Mathematical Model. Bull Math Biol 80(3):540–582. https://doi.org/10.1007/s11538-017-0389-8

    Article  PubMed  Google Scholar 

  16. Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526(7575):666–671. https://doi.org/10.1038/nature15541

    Article  PubMed  Google Scholar 

  17. Wandel MP, Kim BH, Park ES, Boyle KB, Nayak K, Lagrange B, Herod A, Henry T, Zilbauer M, Rohde J, MacMicking JD, Randow F (2020) Guanylate-binding proteins convert cytosolic bacteria into caspase-4 signaling platforms. Nat Immunol 21(8):880–891. https://doi.org/10.1038/s41590-020-0697-2

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gomes MTR, Cerqueira DM, Guimarães ES, Campos PC, Oliveira SC (2019) Guanylate-binding proteins at the crossroad of noncanonical inflammasome activation during bacterial Infections. J Leukoc Biol 106(3):553–562. https://doi.org/10.1002/jlb.4mr0119-013r

    Article  PubMed  Google Scholar 

  19. Yang D, He Y, Munoz-Planillo R, Liu Q, Nunez G (2015) Caspase-11 Requires the Pannexin-1 Channel and the Purinergic P2X7 Pore to Mediate Pyroptosis and Endotoxic Shock. Immunity 43(5):923–932. https://doi.org/10.1016/j.immuni.2015.10.009

    Article  PubMed  PubMed Central  Google Scholar 

  20. Taabazuing CY, Okondo MC, Bachovchin DA (2017) Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in Monocytes and macrophages. Cell Chem Biology 24(4):507–514e504. https://doi.org/10.1016/j.chembiol.2017.03.009

    Article  Google Scholar 

  21. Zhou Z, He H, Wang K, Shi X, Wang Y, Su Y, Wang Y, Li D, Liu W, Zhang Y, Shen L, Han W, Shen L, Ding J, Shao F (2020) Granzyme A from cytotoxic lymphocytes cleaves GSDMB to trigger pyroptosis in target cells. Science 368(6494). https://doi.org/10.1126/science.aaz7548

  22. Zhang Z, Zhang Y, Xia S, Kong Q, Li S, Liu X, Junqueira C, Meza-Sosa KF, Mok TMY, Ansara J, Sengupta S, Yao Y, Wu H, Lieberman J (2020) Gasdermin E suppresses tumour growth by activating anti-tumour immunity. Nature 579(7799):415–420. https://doi.org/10.1038/s41586-020-2071-9

    Article  PubMed  PubMed Central  Google Scholar 

  23. Burgener SS, Leborgne NGF, Snipas SJ, Salvesen GS, Bird PI, Benarafa C (2019) Cathepsin G inhibition by Serpinb1 and Serpinb6 prevents programmed necrosis in neutrophils and monocytes and reduces GSDMD-Driven inflammation. Cell Rep 27(12):3646–3656e3645. https://doi.org/10.1016/j.celrep.2019.05.065

    Article  PubMed  PubMed Central  Google Scholar 

  24. Deng W, Bai Y, Deng F, Pan Y, Mei S, Zheng Z, Min R, Wu Z, Li W, Miao R, Zhang Z, Kupper TS, Lieberman J, Liu X (2022) Streptococcal pyrogenic exotoxin B cleaves GSDMA and triggers pyroptosis. Nature 602(7897):496–502. https://doi.org/10.1038/s41586-021-04384-4

    Article  PubMed  PubMed Central  Google Scholar 

  25. Xu D, Wu X, Peng L, Chen T, Huang Q, Wang Y, Ye C, Peng Y, Hu D, Fang R (2021) The critical role of NLRP6 inflammasome in Streptococcus pneumoniae Infection in Vitro and in vivo. Int J Mol Sci 22(8). https://doi.org/10.3390/ijms22083876

  26. Wang G, Zhang C, Jiang F, Zhao M, Xie S, Liu X (2022) NOD2-RIP2 signaling alleviates microglial ROS damage and pyroptosis via ULK1-mediated autophagy during Streptococcus Pneumonia Infection. Neurosci Lett 783:136743. https://doi.org/10.1016/j.neulet.2022.136743

    Article  PubMed  Google Scholar 

  27. Gou X, Xu W, Liu Y, Peng Y, Xu W, Yin Y, Zhang X (2022) IL-6 prevents lung macrophage death and lung inflammation Injury by inhibiting GSDME- and GSDMD-Mediated pyroptosis during pneumococcal pneumosepsis. Microbiol Spectr 10(2):e0204921. https://doi.org/10.1128/spectrum.02049-21

    Article  PubMed  Google Scholar 

  28. Jung YJ, Pyo S (2015) Pneumococcal protein PspA facilitates Streptococcus Pneumoniae-induced pyrotosis. Faseb J 29(1). https://doi.org/10.1096/fasebj.29.1_supplement.609.3

  29. Fang R, Tsuchiya K, Kawamura I, Shen Y, Hara H, Sakai S, Yamamoto T, Fernandes-Alnemri T, Yang R, Hernandez-Cuellar E, Dewamitta SR, Xu Y, Qu H, Alnemri ES, Mitsuyama M (2011) Critical roles of ASC inflammasomes in caspase-1 activation and host innate resistance to Streptococcus pneumoniae Infection. J Immunol 187(9):4890–4899. https://doi.org/10.4049/jimmunol.1100381

    Article  PubMed  Google Scholar 

  30. Watkins KE, Unnikrishnan M (2020) Evasion of host defenses by intracellular Staphylococcus aureus. Adv Appl Microbiol 112:105–141. https://doi.org/10.1016/bs.aambs.2020.05.001

    Article  PubMed  Google Scholar 

  31. Zhu X, Zhang K, Lu K, Shi T, Shen S, Chen X, Dong J, Gong W, Bao Z, Shi Y, Ma Y, Teng H, Jiang Q (2019) Inhibition of pyroptosis attenuates Staphylococcus aureus-induced bone injury in traumatic osteomyelitis. Annals of Translational Medicine 7(8):170. https://doi.org/10.21037/atm.2019.03.40

    Article  PubMed  PubMed Central  Google Scholar 

  32. Pastar I, Sawaya AP, Marjanovic J, Burgess JL, Strbo N, Rivas KE, Wikramanayake TC, Head CR, Stone RC, Jozic I, Stojadinovic O, Kornfeld EY, Kirsner RS, Lev-Tov H, Tomic-Canic M (2021) Intracellular Staphylococcus aureus triggers pyroptosis and contributes to inhibition of healing due to perforin-2 suppression. J Clin Investig 131(24):e133727. https://doi.org/10.1172/JCI133727

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ghimire L, Paudel S, Jin L, Baral P, Cai S, Jeyaseelan S (2018) NLRP6 negatively regulates pulmonary host defense in Gram-positive bacterial Infection through modulating neutrophil recruitment and function. PLoS Pathog 14(9):e1007308. https://doi.org/10.1371/journal.ppat.1007308

    Article  PubMed  PubMed Central  Google Scholar 

  34. Chow SH, Deo P, Yeung ATY, Kostoulias XP, Jeon Y, Gao ML, Seidi A, Olivier FAB, Sridhar S, Nethercott C, Cameron D, Robertson AAB, Robert R, Mackay CR, Traven A, Jin ZB, Hale C, Dougan G, Peleg AY, Naderer T (2020) Targeting NLRP3 and staphylococcal pore-forming toxin receptors in human-induced pluripotent stem cell-derived macrophages. J Leukoc Biol 108(3):967–981. https://doi.org/10.1002/JLB.4MA0420-497R

    Article  PubMed  Google Scholar 

  35. Wang Y, Zhao N, Jian Y, Liu Y, Zhao L, He L, Liu Q, Li M (2022) The pro-inflammatory effect of Staphylokinase contributes to community-associated Staphylococcus aureus Pneumonia. Commun Biol 5(1):618. https://doi.org/10.1038/s42003-022-03571-x

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hara H, Seregin SS, Yang D, Fukase K, Chamaillard M, Alnemri ES, Inohara N, Chen GY, Nunez G (2018) The NLRP6 Inflammasome recognizes Lipoteichoic Acid and regulates gram-positive Pathogen Infection. Cell 175(6):1651–1664e1614. https://doi.org/10.1016/j.cell.2018.09.047

    Article  PubMed  PubMed Central  Google Scholar 

  37. Soong G, Chun J, Parker D, Prince A (2012) Staphylococcus aureus activation of caspase 1/calpain signaling mediates invasion through human keratinocytes. J Infect Dis 205(10):1571–1579. https://doi.org/10.1093/infdis/jis244

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gram AM, Wright JA, Pickering RJ, Lam NL, Booty LM, Webster SJ, Bryant CE (2021) Salmonella flagellin activates NAIP/NLRC4 and canonical NLRP3 inflammasomes in human macrophages. J Immunol 206(3):631–640. https://doi.org/10.4049/jimmunol.2000382

    Article  PubMed  Google Scholar 

  39. Naseer N, Egan MS, Reyes Ruiz VM, Scott WP, Hunter EN, Demissie T, Rauch I, Brodsky IE, Shin S (2022) Human NAIP/NLRC4 and NLRP3 inflammasomes detect Salmonella type III secretion system activities to restrict intracellular bacterial replication. PLoS Pathog 18(1):e1009718. https://doi.org/10.1371/journal.ppat.1009718

    Article  PubMed  PubMed Central  Google Scholar 

  40. Knodler LA, Crowley SM, Sham HP, Yang H, Wrande M, Ma C, Ernst RK, Steele-Mortimer O, Celli J, Vallance BA (2014) Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16(2):249–256. https://doi.org/10.1016/j.chom.2014.07.002

    Article  PubMed  PubMed Central  Google Scholar 

  41. Santos JC, Boucher D, Schneider LK, Demarco B, Dilucca M, Shkarina K, Heilig R, Chen KW, Lim RYH, Broz P (2020) Human GBP1 binds LPS to initiate assembly of a caspase-4 activating platform on cytosolic bacteria. Nat Commun 11(1):3276. https://doi.org/10.1038/s41467-020-16889-z

    Article  PubMed  PubMed Central  Google Scholar 

  42. Mitchell PS, Roncaioli JL, Turcotte EA, Goers L, Chavez RA, Lee AY, Lesser CF, Rauch I, Vance RE (2020) NAIP-NLRC4-deficient mice are susceptible to shigellosis. eLife 9. https://doi.org/10.7554/eLife.59022

  43. Philpott DJ, Suzuki S, Franchi L, He Y, Muñoz-Planillo R, Mimuro H, Suzuki T, Sasakawa C, Núñez G (2014) Shigella Type III secretion protein MxiI is recognized by Naip2 to Induce Nlrc4 inflammasome activation independently of Pkcδ. PLoS Pathog 10(2). https://doi.org/10.1371/journal.ppat.1003926

  44. Suzuki S, Suzuki T, Mimuro H, Mizushima T, Sasakawa C (2018) Shigella hijacks the glomulin-cIAPs-inflammasome axis to promote inflammation. EMBO Rep 19(1):89–101. https://doi.org/10.15252/embr.201643841

    Article  PubMed  Google Scholar 

  45. Wang X, Sun J, Wan L, Yang X, Lin H, Zhang Y, He X, Zhong H, Guan K, Min M, Sun Z, Yang X, Wang B, Dong M, Wei C (2020) The Shigella type III secretion Effector IpaH4.5 targets NLRP3 to activate Inflammasome Signaling. Front Cell Infect Microbiol 10. https://doi.org/10.3389/fcimb.2020.511798

  46. Beckwith KS, Beckwith MS, Ullmann S, Saetra RS, Kim H, Marstad A, Asberg SE, Strand TA, Haug M, Niederweis M, Stenmark HA, Flo TH (2020) Plasma membrane damage causes NLRP3 activation and pyroptosis during Mycobacterium tuberculosis Infection. Nat Commun 11(1):2270. https://doi.org/10.1038/s41467-020-16143-6

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gong Z, Kuang Z, Li H, Li C, Ali MK, Huang F, Li P, Li Q, Huang X, Ren S, Li J, Xie J (2019) Regulation of host cell pyroptosis and cytokines production by Mycobacterium tuberculosis effector PPE60 requires LUBAC mediated NF-κB signaling. Cell Immunol 335:41–50. https://doi.org/10.1016/j.cellimm.2018.10.009

    Article  PubMed  Google Scholar 

  48. Li Y, Fu Y, Sun J, Shen J, Liu F, Ning B, Lu Z, Wei L, Jiang X (2022) Tanshinone IIA alleviates NLRP3 inflammasome-mediated pyroptosis in Mycobacterium tuberculosis-(H37Ra-) infected macrophages by inhibiting endoplasmic reticulum stress. J Ethnopharmacol 282:114595. https://doi.org/10.1016/j.jep.2021.114595

    Article  PubMed  Google Scholar 

  49. Qian J, Hu Y, Zhang X, Chi M, Xu S, Wang H, Zhang X (2022) Mycobacterium tuberculosis PE_PGRS19 induces pyroptosis through a non-classical Caspase-11/GSDMD pathway in macrophages. Microorganisms 10(12). https://doi.org/10.3390/microorganisms10122473

  50. Sugiyama M, Saeki A, Hasebe A, Kamesaki R, Yoshida Y, Kitagawa Y, Suzuki T, Shibata K (2016) Activation of inflammasomes in dendritic cells and macrophages by Mycoplasma salivarium. Mol Oral Microbiol 31(3):259–269. https://doi.org/10.1111/omi.12117

    Article  PubMed  Google Scholar 

  51. Segovia JA, Chang TH, Winter VT, Coalson JJ, Cagle MP, Pandranki L, Bose S, Baseman JB, Kannan TR (2018) NLRP3 is a critical Regulator of inflammation and Innate Immune Cell response during Mycoplasma pneumoniae Infection. Infect Immun 86(1):e00548–e00517. https://doi.org/10.1128/IAI.00548-17

    Article  PubMed  Google Scholar 

  52. Liu F, Liu T, Sun M, Zhou J, Xue F, Chen S, Chen J, Zhang L (2021) Maxing Shigan Decoction mitigates Mycoplasma pneumonia-Induced pyroptosis in A549 cells via the NLRP3 inflammasome. Infect Drug Resist 14:859–867. https://doi.org/10.2147/idr.S292413

    Article  PubMed  PubMed Central  Google Scholar 

  53. Liu X, Lin Z, Yin X (2022) Pellino2 accelerate inflammation and pyroptosis via the ubiquitination and activation of NLRP3 inflammation in model of pediatric Pneumonia. Int Immunopharmacol 110:108993. https://doi.org/10.1016/j.intimp.2022.108993

    Article  PubMed  Google Scholar 

  54. Tan TY, Chu JJH (2013) Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol 94(Pt 10):2215–2220. https://doi.org/10.1099/vir.0.055277-0

    Article  PubMed  Google Scholar 

  55. Cheung KT, Sze DM, Chan KH, Leung PH (2018) Involvement of caspase-4 in IL-1 beta production and pyroptosis in human macrophages during dengue virus Infection. Immunobiology 223(4–5):356–364. https://doi.org/10.1016/j.imbio.2017.10.044

    Article  PubMed  Google Scholar 

  56. Wu MF, Chen ST, Yang AH, Lin WW, Lin YL, Chen NJ, Tsai IS, Li L, Hsieh SL (2013) CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood 121(1):95–106. https://doi.org/10.1182/blood-2012-05-430090

    Article  PubMed  Google Scholar 

  57. Lien TS, Sun DS, Wu CY, Chang HH (2021) Exposure to Dengue envelope protein domain III induces Nlrp3 inflammasome-dependent endothelial dysfunction and Hemorrhage in mice. Front Immunol 12:617251. https://doi.org/10.3389/fimmu.2021.617251

    Article  PubMed  PubMed Central  Google Scholar 

  58. Lien TS, Sun DS, Hung SC, Wu WS, Chang HH (2021) Dengue Virus envelope protein domain III induces Nlrp3 inflammasome-dependent NETosis-Mediated inflammation in mice. Front Immunol 12:618577. https://doi.org/10.3389/fimmu.2021.618577

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wei KC, Wei WJ, Liao CL, Chang TH (2023) Discrepant activation pattern of inflammation and pyroptosis Induced in dermal fibroblasts in response to Dengue Virus Serotypes 1 and 2 and nonstructural protein 1. Microbiol Spectr 11(1):e0358622. https://doi.org/10.1128/spectrum.03586-22

    Article  PubMed  Google Scholar 

  60. Fernandez MV, Miller E, Krammer F, Gopal R, Greenbaum BD, Bhardwaj N (2016) Ion efflux and Influenza Infection trigger NLRP3 inflammasome signaling in human dendritic cells. J Leukoc Biol 99(5):723–734. https://doi.org/10.1189/jlb.3A0614-313RRR

    Article  PubMed  Google Scholar 

  61. Mishra S, Raj AS, Kumar A, Rajeevan A, Kumari P, Kumar H (2022) Innate immune sensing of Influenza a viral RNA through IFI16 promotes pyroptotic cell death. iScience 25(1):103714. https://doi.org/10.1016/j.isci.2021.103714

    Article  PubMed  Google Scholar 

  62. Kuriakose T, Man SM, Malireddi RK, Karki R, Kesavardhana S, Place DE, Neale G, Vogel P, Kanneganti TD (2016) ZBP1/DAI is an innate sensor of Influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways. Sci Immunol 1(2):aag2045. https://doi.org/10.1126/sciimmunol.aag2045

    Article  PubMed  PubMed Central  Google Scholar 

  63. Zheng M, Karki R, Vogel P, Kanneganti TD (2020) Caspase-6 is a Key Regulator of Innate Immunity, Inflammasome activation, and Host Defense. Cell 181(3):674–687e613. https://doi.org/10.1016/j.cell.2020.03.040

    Article  PubMed  PubMed Central  Google Scholar 

  64. Wan X, Li J, Wang Y, Yu X, He X, Shi J, Deng G, Zeng X, Tian G, Li Y, Jiang Y, Guan Y, Li C, Shao F, Chen H (2022) H7N9 virus Infection triggers lethal cytokine Storm by activating gasdermin E-mediated pyroptosis of lung alveolar epithelial cells. Natl Sci Rev 9(1):nwab137. https://doi.org/10.1093/nsr/nwab137

    Article  PubMed  Google Scholar 

  65. Cai W, Wu LR, Zhang SL (2022) Lignans from Mosla scabra Ameliorated Influenza A Virus-Induced Pneumonia via Inhibiting Macrophage Activation. Evid Based Complement Alternat Med 2022:1688826. https://doi.org/10.1155/2022/1688826

  66. Ferreira AC, Soares VC, de Azevedo-Quintanilha IG, Dias S, Fintelman-Rodrigues N, Sacramento CQ, Mattos M, de Freitas CS, Temerozo JR, Teixeira L, Damaceno Hottz E, Barreto EA, Pao CRR, Palhinha L, Miranda M, Bou-Habib DC, Bozza FA, Bozza PT, Souza TML (2021) SARS-CoV-2 engages inflammasome and pyroptosis in human primary monocytes. Cell Death Discov 7(1):43. https://doi.org/10.1038/s41420-021-00428-w

    Article  PubMed  PubMed Central  Google Scholar 

  67. Zhang J, Wu H, Yao X, Zhang D, Zhou Y, Fu B, Wang W, Li H, Wang Z, Hu Z, Ren Y, Sun R, Tian Z, Bian X, Wei H (2021) Pyroptotic macrophages stimulate the SARS-CoV-2-associated cytokine Storm. Cell Mol Immunol 18(5):1305–1307. https://doi.org/10.1038/s41423-021-00665-0

    Article  PubMed  PubMed Central  Google Scholar 

  68. Tong X, Ping HQ, Gong XM, Zhang K, Chen ZJ, Cai CY, Lu ZY, Yang RR, Gao SC, Wang YY, Wang XH, Liu L, Ke HN (2022) Pyroptosis in the lung and spleen of patients died from COVID-19. Eur J Inflamm 20. https://doi.org/10.1177/1721727x221140661

  69. Planes R, Pinilla M, Santoni K, Hessel A, Passemar C, Lay K, Paillette P, Valadao AC, Robinson KS, Bastard P, Lam N, Fadrique R, Rossi I, Pericat D, Bagayoko S, Leon-Icaza SA, Rombouts Y, Perouzel E, Tiraby M, Effort CHG, Zhang Q, Cicuta P, Jouanguy E, Neyrolles O, Bryant CE, Floto AR, Goujon C, Lei FZ, Martin-Blondel G, Silva S, Casanova JL, Cougoule C, Reversade B, Marcoux J, Ravet E, Meunier E (2022) Human NLRP1 is a sensor of pathogenic coronavirus 3CL proteases in lung epithelial cells. Mol Cell 82(13):2385–2400 e2389. https://doi.org/10.1016/j.molcel.2022.04.033

  70. Chen IY, Moriyama M, Chang MF, Ichinohe T (2019) Severe Acute Respiratory Syndrome Coronavirus Viroporin 3a activates the NLRP3 inflammasome. Front Microbiol 10:50. https://doi.org/10.3389/fmicb.2019.00050

    Article  PubMed  PubMed Central  Google Scholar 

  71. Gowda P, Patrick S, Joshi SD, Kumawat RK, Sen E (2021) Glycyrrhizin prevents SARS-CoV-2 S1 and Orf3a induced high mobility group box 1 (HMGB1) release and inhibits viral replication. Cytokine 142:155496. https://doi.org/10.1016/j.cyto.2021.155496

    Article  PubMed  PubMed Central  Google Scholar 

  72. Sun X, Liu Y, Huang Z, Xu W, Hu W, Yi L, Liu Z, Chan H, Zeng J, Liu X, Chen H, Yu J, Chan FKL, Ng SC, Wong SH, Wang MH, Gin T, Joynt GM, Hui DSC, Zou X, Shu Y, Cheng CHK, Fang S, Luo H, Lu J, Chan MTV, Zhang L, Wu WKK (2022) SARS-CoV-2 non-structural protein 6 triggers NLRP3-dependent pyroptosis by targeting ATP6AP1. Cell Death Differ 29(6):1240–1254. https://doi.org/10.1038/s41418-021-00916-7

    Article  PubMed  PubMed Central  Google Scholar 

  73. Ma H, Zhu Z, Lin H, Wang S, Zhang P, Li Y, Li L, Wang J, Zhao Y, Han J (2021) Pyroptosis of syncytia formed by fusion of SARS-CoV-2 spike and ACE2-expressing cells. Cell Discov 7(1):73. https://doi.org/10.1038/s41421-021-00310-0

    Article  PubMed  PubMed Central  Google Scholar 

  74. Ji Q, Wang L, Liu J, Wu Y, Lv H, Wen Y, Shi L, Qu B, Szentmary N (2021) Aspergillus fumigatus-stimulated human corneal epithelial cells induce pyroptosis of THP-1 macrophages by secreting TSLP. Inflammation 44(2):682–692. https://doi.org/10.1007/s10753-020-01367-x

    Article  PubMed  Google Scholar 

  75. Karki R, Man SM, Malireddi RKS, Gurung P, Vogel P, Lamkanfi M, Kanneganti TD (2015) Concerted activation of the AIM2 and NLRP3 inflammasomes orchestrates host protection against aspergillus Infection. Cell Host Microbe 17(3):357–368. https://doi.org/10.1016/j.chom.2015.01.006

    Article  PubMed  PubMed Central  Google Scholar 

  76. Wang L, Yan H, Chen X, Lee J, Sun J, Liu G, Yang H, Lu D, Liu W, Che C (2022) Caspase-8 is involved in pyroptosis, necroptosis and the maturation and release of IL-1β in aspergillus fumigatus keratitis. Int Immunopharmacol 113(Pt A):109275. https://doi.org/10.1016/j.intimp.2022.109275

    Article  PubMed  Google Scholar 

  77. Yan W, Zhao YS, Xie K, Xing Y, Xu F (2021) Aspergillus fumigatus Influences Gasdermin-D-Dependent Pyroptosis of the Lung via Regulating Toll-Like Receptor 2-Mediated Regulatory T Cell Differentiation. J Immunol Res 2021:5538612. https://doi.org/10.1155/2021/5538612

  78. Zhao W, Yang H, Lyu L, Zhang J, Xu Q, Jiang N, Liu G, Wang L, Yan H, Che C (2021) GSDMD, an executor of pyroptosis, is involved in IL-1beta secretion in aspergillus fumigatus keratitis. Exp Eye Res 202:108375. https://doi.org/10.1016/j.exer.2020.108375

    Article  PubMed  Google Scholar 

  79. Chen M, Xing Y, Lu A, Fang W, Sun B, Chen C, Liao W, Meng G (2015) Internalized Cryptococcus neoformans activates the Canonical Caspase-1 and the Noncanonical Caspase-8 inflammasomes. J Immunol 195(10):4962–4972. https://doi.org/10.4049/jimmunol.1500865

    Article  PubMed  Google Scholar 

  80. Wang Y, Feng F, Wang H, Zhang Y, Chen Y (2022) The Inflammasome NLRC4 protects against Cryptococcus gattii by inducing the Classic Caspase-1 to activate the Pyroptosis Signal. J Healthc Eng 2022:7355485. https://doi.org/10.1155/2022/7355485

    Article  PubMed  PubMed Central  Google Scholar 

  81. Wellington M, Koselny K, Sutterwala FS, Krysan DJ (2014) Candida albicans triggers NLRP3-mediated pyroptosis in macrophages. Eukaryot Cell 13(2):329–340. https://doi.org/10.1128/EC.00336-13

    Article  PubMed  PubMed Central  Google Scholar 

  82. Frank D, Naseem S, Russo GL, Li C, Parashar K, Konopka JB, Carpino N (2018) Phagocytes from mice lacking the Sts Phosphatases have an enhanced antifungal response to Candida albicans. mBio 9(4). https://doi.org/10.1128/mBio.00782-18

  83. Banoth B, Tuladhar S, Karki R, Sharma BR, Briard B, Kesavardhana S, Burton A, Kanneganti TD (2020) ZBP1 promotes fungi-induced inflammasome activation and pyroptosis, apoptosis, and necroptosis (PANoptosis). J Biol Chem 295(52):18276–18283. https://doi.org/10.1074/jbc.RA120.015924

    Article  PubMed  Google Scholar 

  84. Bhatt B, Prakhar P, Lohia GK, Rajmani RS, Balaji KN (2022) Pre-existing mycobacterial Infection modulates Candida albicans-driven pyroptosis. FEBS J 289(6):1536–1551. https://doi.org/10.1111/febs.16243

    Article  PubMed  Google Scholar 

  85. O’Meara TR, Duah K, Guo CX, Maxson ME, Gaudet RG, Koselny K, Wellington M, Powers ME, MacAlpine J, O’Meara MJ, Veri AO, Grinstein S, Noble SM, Krysan D, Gray-Owen SD, Cowen LE (2018) High-throughput screening identifies genes required for Candida albicans induction of macrophage pyroptosis. mBio 9(4). https://doi.org/10.1128/mBio.01581-18

  86. Koselny K, Mutlu N, Minard AY, Kumar A, Krysan DJ, Wellington M (2018) A genome-wide screen of deletion mutants in the Filamentous Saccharomyces cerevisiae background identifies ergosterol as a direct trigger of macrophage pyroptosis. mBio 9(4):e01204–01218. https://doi.org/10.1128/mBio.01204-18

    Article  PubMed  PubMed Central  Google Scholar 

  87. Kasper L, Konig A, Koenig PA, Gresnigt MS, Westman J, Drummond RA, Lionakis MS, Gross O, Ruland J, Naglik JR, Hube B (2018) The fungal peptide toxin Candidalysin activates the NLRP3 inflammasome and causes cytolysis in mononuclear phagocytes. Nat Commun 9(1):4260. https://doi.org/10.1038/s41467-018-06607-1

    Article  PubMed  PubMed Central  Google Scholar 

  88. Zuo L, Zhou L, Wu C, Wang Y, Li Y, Huang R, Wu S (2020) Salmonella spvC gene inhibits pyroptosis and intestinal inflammation to aggravate Systemic Infection in mice. Front Microbiol 11:562491. https://doi.org/10.3389/fmicb.2020.562491

    Article  PubMed  PubMed Central  Google Scholar 

  89. Yuan H, Zhou L, Chen Y, You J, Hu H, Li Y, Huang R, Wu S (2023) Salmonella effector SopF regulates PANoptosis of intestinal epithelial cells to aggravate Systemic Infection. Gut Microbes 15(1):2180315. https://doi.org/10.1080/19490976.2023.2180315

    Article  PubMed  PubMed Central  Google Scholar 

  90. Mylona E, Sanchez-Garrido J, Hoang Thu TN, Dongol S, Karkey A, Baker S, Shenoy AR, Frankel G (2021) Very long O-antigen chains of Salmonella Paratyphi a inhibit inflammasome activation and pyroptotic cell death. Cell Microbiol 23(5):e13306. https://doi.org/10.1111/cmi.13306

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rastogi S, Ellinwood S, Augenstreich J, Mayer-Barber KD, Briken V (2021) Mycobacterium tuberculosis inhibits the NLRP3 inflammasome activation via its phosphokinase PknF. PLoS Pathog 17(7):e1009712. https://doi.org/10.1371/journal.ppat.1009712

    Article  PubMed  PubMed Central  Google Scholar 

  92. Bürgel PH, Marina CL, Saavedra PHV, Albuquerque P, de Oliveira SAM, Veloso Janior PHH, de Castro RA, Heyman HM, Coelho C, Cordero RJB, Casadevall A, Nosanchuk JD, Nakayasu ES, May RC, Tavares AH, Bocca AL (2020) Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion. Mediators Inflamm 2020:3412763. https://doi.org/10.1155/2020/3412763

  93. Li Z, Liu W, Fu J, Cheng S, Xu Y, Wang Z, Liu X, Shi X, Liu Y, Qi X, Liu X, Ding J, Shao F (2021) Shigella evades pyroptosis by arginine ADP-riboxanation of caspase-11. Nature 599(7884):290–295. https://doi.org/10.1038/s41586-021-04020-1

    Article  PubMed  Google Scholar 

  94. Luchetti G, Roncaioli JL, Chavez RA, Schubert AF, Kofoed EM, Reja R, Cheung TK, Liang Y, Webster JD, Lehoux I, Skippington E, Reeder J, Haley B, Tan MW, Rose CM, Newton K, Kayagaki N, Vance RE, Dixit VM (2021) Shigella ubiquitin ligase IpaH7.8 targets gasdermin D for degradation to prevent pyroptosis and enable Infection. Cell Host Microbe 29(10):1521–1530e1510. https://doi.org/10.1016/j.chom.2021.08.010

    Article  PubMed  PubMed Central  Google Scholar 

  95. Chai Q, Yu S, Zhong Y, Lu Z, Qiu C, Yu Y, Zhang X, Zhang Y, Lei Z, Qiang L, Li BX, Pang Y, Qiu XB, Wang J, Liu CH (2022) A bacterial phospholipid phosphatase inhibits host pyroptosis by Hijacking ubiquitin. Science 378(6616):eabq0132. https://doi.org/10.1126/science.abq0132

    Article  PubMed  Google Scholar 

  96. Ma J, Zhu F, Zhao M, Shao F, Yu D, Ma J, Zhang X, Li W, Qian Y, Zhang Y, Jiang D, Wang S, Xia P (2021) SARS-CoV-2 nucleocapsid suppresses host pyroptosis by blocking gasdermin D cleavage. EMBO J 40(18):e108249. https://doi.org/10.15252/embj.2021108249

    Article  PubMed  PubMed Central  Google Scholar 

  97. Shi F, Lv Q, Wang T, Xu J, Xu W, Shi Y, Fu X, Yang T, Yang Y, Zhuang L, Fang W, Gu J, Li X (2022) Coronaviruses Nsp5 antagonizes porcine gasdermin D-Mediated pyroptosis by cleaving pore-forming p30 fragment. mBio 13(1):e0273921. https://doi.org/10.1128/mbio.02739-21

    Article  PubMed  Google Scholar 

  98. Peng Y, Wang X, Wang H, Xu W, Wu K, Go X, Yin Y, Zhang X (2021) Interleukin-4 protects mice against lethal Influenza and Streptococcus pneumoniae co-infected Pneumonia. Clin Exp Immunol 205(3):379–390. https://doi.org/10.1111/cei.13628

    Article  PubMed  PubMed Central  Google Scholar 

  99. Xiong S, Zhang L, Richner JM, Class J, Rehman J, Malik AB (2021) Interleukin-1RA mitigates SARS-CoV-2-Induced inflammatory lung vascular leakage and mortality in Humanized K18-hACE-2 mice. Arterioscler Thromb Vasc Biol 41(11):2773–2785. https://doi.org/10.1161/ATVBAHA.121.316925

    Article  PubMed  PubMed Central  Google Scholar 

  100. Tate MD, Ong JDH, Dowling JK, McAuley JL, Robertson AB, Latz E, Drummond GR, Cooper MA, Hertzog PJ, Mansell A (2016) Reassessing the role of the NLRP3 inflammasome during pathogenic Influenza a virus Infection via temporal inhibition. Sci Rep 6:27912. https://doi.org/10.1038/srep27912

    Article  PubMed  PubMed Central  Google Scholar 

  101. Saeedi-Boroujeni A, Nashibi R, Ghadiri AA, Nakajima M, Salmanzadeh S, Mahmoudian-Sani MR, Hanafi MG, Sharhani A, Khodadadi A (2022) Tranilast as an adjunctive therapy in hospitalized patients with severe COVID- 19: a Randomized Controlled Trial. Arch Med Res 53(4):368–377. https://doi.org/10.1016/j.arcmed.2022.03.002

    Article  PubMed  PubMed Central  Google Scholar 

  102. Lien TS, Chan H, Sun DS, Wu JC, Lin YY, Lin GL, Chang HH (2021) Exposure of platelets to Dengue Virus and envelope protein domain III induces Nlrp3 inflammasome-dependent platelet cell death and Thrombocytopenia in mice. Front Immunol 12:616394. https://doi.org/10.3389/fimmu.2021.616394

    Article  PubMed  PubMed Central  Google Scholar 

  103. Gu L, Lin J, Wang Q, Zhang L, Yin M, Lin H, Zheng H, Zhao G, Li C (2023) Dimethyl fumarate ameliorates fungal keratitis by limiting fungal growth and inhibiting pyroptosis. Int Immunopharmacol 115:109721. https://doi.org/10.1016/j.intimp.2023.109721

    Article  PubMed  Google Scholar 

  104. Yan H, Yang H, Wang L, Sun X, Han L, Cong P, Chen X, Lu D, Che C (2022) Disulfiram inhibits IL-1beta secretion and inflammatory cells recruitment in aspergillus fumigatus keratitis. Int Immunopharmacol 102:108401. https://doi.org/10.1016/j.intimp.2021.108401

    Article  PubMed  Google Scholar 

  105. Ryan TAJ, Hooftman A, Rehill AM, Johansen MD, Brien ECO, Toller-Kawahisa JE, Wilk MM, Day EA, Weiss HJ, Sarvari P, Vozza EG, Schramm F, Peace CG, Zotta A, Miemczyk S, Nalkurthi C, Hansbro NG, McManus G, O’Doherty L, Gargan S, Long A, Dunne J, Cheallaigh CN, Conlon N, Carty M, Fallon PG, Mills KHG, Creagh EM, Donnell JSO, Hertzog PJ, Hansbro PM, McLoughlin RM, Wygrecka M, Preston RJS, Zasłona Z (2023) L.A.J. O’Neill Dimethyl fumarate and 4-octyl itaconate are anticoagulants that suppress Tissue Factor in macrophages via inhibition of Type I Interferon. Nat Commun 14(1):3513. https://doi.org/10.1038/s41467-023-39174-1

  106. Adrover JM, Carrau L, Dassler-Plenker J, Bram Y, Chandar V, Houghton S, Redmond D, Merrill JR, Shevik M, tenOever BR, Lyons SK, Schwartz RE, Egeblad M (2022) Disulfiram inhibits neutrophil extracellular trap formation and protects rodents from acute lung injury and SARS-CoV-2 Infection. JCI Insight 7(5):e157342. https://doi.org/10.1172/jci.insight.157342

    Article  PubMed  PubMed Central  Google Scholar 

  107. Tang Z, Liu S, Chen N, Luo M, Wu J, Zheng Y (2021) Gold nanoclusters treat intracellular bacterial Infections: eliminating phagocytic pathogens and regulating cellular immune response. Colloids Surf B Biointerfaces 205:111899. https://doi.org/10.1016/j.colsurfb.2021.111899

    Article  PubMed  Google Scholar 

  108. Yao L, Sun T (2019) Glycyrrhizin administration ameliorates Streptococcus aureus-induced acute lung injury. Int Immunopharmacol 70:504–511. https://doi.org/10.1016/j.intimp.2019.02.046

    Article  PubMed  Google Scholar 

  109. An C, Wu Y, Wu J, Liu H, Zhou S, Ge D, Dong R, You L, Hao Y (2022) Berberine ameliorates pulmonary inflammation in mice with Influenza viral Pneumonia by inhibiting NLRP3 inflammasome activation and gasdermin D-mediated pyroptosis. Drug Dev Res 83(7):1707–1721. https://doi.org/10.1002/ddr.21995

    Article  PubMed  Google Scholar 

  110. Xu MM, Kang JY, Ji S, Wei YY, Wei SL, Ye JJ, Wang YG, Shen JL, Wu HM, Fei GH (2022) Melatonin Suppresses Macrophage M1 Polarization and ROS-Mediated Pyroptosis via Activating ApoE/LDLR Pathway in Influenza A-Induced Acute Lung Injury. Oxid Med Cell Longev 2022:2520348. https://doi.org/10.1155/2022/2520348

Download references

Funding

This work was supported by the Natural Science Foundation of Hunan Province (2020JJ4527, 2023JJ30501, 2023JJ30502) and the Scientific Research Fund of Hunan Provincial Education Department (21B0399).

Author information

Authors and Affiliations

  1. Department of Public Health Laboratory Sciences, School of Public Health, Hengyang Medical School, University of South China, Hengyang, Hunan, 421001, China

    Cui Xiao, Saihong Cao, Yunfei Li, Yuchen Luo, Jian Liu, Qinqin Bai & Lili Chen

  2. Yiyang Medical College, School of Public Health and Laboratory Medicine, Yiyang, Hunan, 421000, China

    Saihong Cao

  3. The Affiliated Cancer Hospital of Xiangya School of Medicine, Hunan Cancer Hospital, Central South University Infection-Associated Hemophagocytic Syndrome, Changsha, Hunan, 421000, China

    Yuyu Chen

Authors
  1. Cui Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saihong Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunfei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuchen Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuyu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qinqin Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lili Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Cui Xiao had the idea for the article and drafted the manuscript. Cui Xiao, Saihong Cao, Yunfei Li, Yuchen Luo, Jian Liu, Yuyu Chen, Qinqin Bai, and Lili Chen performed the literature search and revised the manuscript. Lili Chen and Qinqin Bai critically revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Qinqin Bai or Lili Chen.

Ethics declarations

Conflict of interest

The authors have no financial conflict of interest.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, C., Cao, S., Li, Y. et al. Pyroptosis in microbial infectious diseases. Mol Biol Rep 51, 42 (2024). https://doi.org/10.1007/s11033-023-09078-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11033-023-09078-w

Keywords

Search

Navigation