IMMUNE NETWORK

  • 제21권5호
  • /
  • Pages.36.1-36.16
  • /
  • 2021
  • /
  • 1598-2629(pISSN)
  • /
  • 2092-6685(eISSN)
대한면역학회 (The Korean Association of Immunobiologists)
권호 표지
DOI QR코드

DOI QR Code

Inflammasome-Dependent Peroxiredoxin 2 Secretion Induces the Classical Complement Pathway Activation

  • Cheol Ho Park (Department of Microbiology, Yonsei University College of Medicine) ;
  • Hyun Sook Lee (Department of Microbiology, Yonsei University College of Medicine) ;
  • Man Sup Kwak (Department of Microbiology, Yonsei University College of Medicine) ;
  • Jeon-Soo Shin (Department of Microbiology, Yonsei University College of Medicine)
  • 투고 : 2021.07.28
  • 심사 : 2021.09.08
  • 발행 : 2021.10.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Peroxiredoxins (Prxs) are ubiquitously expressed peroxidases that reduce hydrogen peroxide or alkyl peroxide production in cells. Prxs are released from cells in response to various stress conditions, and they function as damage-associated molecular pattern molecules. However, the secretory mechanism of Prxs and their roles have not been elucidated. Thus, we aimed to determine whether inflammasome activation is a secretory mechanism of Prxs and subsequently identify the effect of the secreted Prxs on activation of the classical complement pathway. Using J774A.1, a murine macrophage cell line, we demonstrated that NLRP3 inflammasome activation induces Prx1, Prx2, Prx5, and Prx6 secretion in a caspase-1 dependent manner. Using HEK293T cells with a transfection system, we revealed that the release of Prx1 and Prx2 relies on gasdermin-D (GSDMD)-mediated secretion. Next, we confirmed the binding of both Prx1 and Prx2 to C1q; however, only Prx2 could induce the C1q-mediated classical complement pathway activation. Collectively, our results suggest that inflammasome activation is a secretory mechanism of Prxs and that GSDMD is a mediator of their secretion. Moreover, secreted Prx1 and Prx2 bind with C1q, but only Prx2 mediates the classical complement pathway activation.

키워드

과제정보

We thank Sook Young Kim for the help of complement-related assay. This work was supported by grants from the National Research Foundation of Korea (NRF) funded by the Korean government (No. 2017R1A2B3006704, 2019R1A6A1A03032869, 2021R1I1A1A01044809).

참고문헌

  1. Cox AG, Winterbourn CC, Hampton MB. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 2009;425:313-325. https://doi.org/10.1042/BJ20091541
  2. Lee S, Wi SM, Min Y, Lee KY. Peroxiredoxin-3 is involved in bactericidal activity through the regulation of mitochondrial reactive oxygen species. Immune Netw 2016;16:373-380. https://doi.org/10.4110/in.2016.16.6.373
  3. Neumann CA, Krause DS, Carman CV, Das S, Dubey DP, Abraham JL, Bronson RT, Fujiwara Y, Orkin SH, Van Etten RA. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 2003;424:561-565. https://doi.org/10.1038/nature01819
  4. Lee TH, Kim SU, Yu SL, Kim SH, Park DS, Moon HB, Dho SH, Kwon KS, Kwon HJ, Han YH, et al. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 2003;101:5033-5038. https://doi.org/10.1182/blood-2002-08-2548
  5. Perricone C, De Carolis C, Perricone R. Glutathione: a key player in autoimmunity. Autoimmun Rev 2009;8:697-701. https://doi.org/10.1016/j.autrev.2009.02.020
  6. Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, Takada I, Sekiya T, Ooboshi H, Kitazono T, Yanagawa T, et al. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat Med 2012;18:911-917. https://doi.org/10.1038/nm.2749
  7. Salzano S, Checconi P, Hanschmann EM, Lillig CH, Bowler LD, Chan P, Vaudry D, Mengozzi M, Coppo L, Sacre S, et al. Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc Natl Acad Sci U S A 2014;111:12157-12162. https://doi.org/10.1073/pnas.1401712111
  8. He Y, Li S, Tang D, Peng Y, Meng J, Peng S, Deng Z, Qiu S, Liao X, Chen H, et al. Circulating peroxiredoxin-1 is a novel damage-associated molecular pattern and aggravates acute liver injury via promoting inflammation. Free Radic Biol Med 2019;137:24-36. https://doi.org/10.1016/j.freeradbiomed.2019.04.012
  9. Schroder K, Tschopp J. The inflammasomes. Cell 2010;140:821-832. https://doi.org/10.1016/j.cell.2010.01.040
  10. Feng S, Fox D, Man SM. Mechanisms of gasdermin family members in inflammasome signaling and cell death. J Mol Biol 2018;430:3068-3080. https://doi.org/10.1016/j.jmb.2018.07.002
  11. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, Sun H, Wang DC, Shao F. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 2016;535:111-116. https://doi.org/10.1038/nature18590
  12. Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 2016;535:153-158. https://doi.org/10.1038/nature18629
  13. Walport MJ. Complement. First of two parts. N Engl J Med 2001;344:1058-1066. https://doi.org/10.1056/NEJM200104053441406
  14. Walport MJ. Complement. Second of two parts. N Engl J Med 2001;344:1140-1144. https://doi.org/10.1056/NEJM200104123441506
  15. Paidassi H, Tacnet-Delorme P, Garlatti V, Darnault C, Ghebrehiwet B, Gaboriaud C, Arlaud GJ, Frachet P. C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J Immunol 2008;180:2329-2338. https://doi.org/10.4049/jimmunol.180.4.2329
  16. Kang YH, Tan LA, Carroll MV, Gentle ME, Sim RB. Target pattern recognition by complement proteins of the classical and alternative pathways. Adv Exp Med Biol 2009;653:117-128. https://doi.org/10.1007/978-1-4419-0901-5_8
  17. Kim SY, Son M, Lee SE, Park IH, Kwak MS, Han M, Lee HS, Kim ES, Kim JY, Lee JE, et al. High-mobility group box 1-induced complement activation causes sterile inflammation. Front Immunol 2018;9:705.
  18. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008;9:847-856. https://doi.org/10.1038/ni.1631
  19. Kaplan MH, Volanakis JE. Interaction of C-reactive protein complexes with the complement system. I. Consumption of human complement associated with the reaction of C-reactive protein with pneumococcal C-polysaccharide and with the choline phosphatides, lecithin and sphingomyelin. J Immunol 1974;112:2135-2147. https://doi.org/10.4049/jimmunol.112.6.2135
  20. Bhakdi S, Torzewski M, Paprotka K, Schmitt S, Barsoom H, Suriyaphol P, Han SR, Lackner KJ, Husmann M. Possible protective role for C-reactive protein in atherogenesis: complement activation by modified lipoproteins halts before detrimental terminal sequence. Circulation 2004;109:1870-1876. https://doi.org/10.1161/01.CIR.0000124228.08972.26
  21. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015;526:660-665.  https://doi.org/10.1038/nature15514
  22. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 2015;526:666-671. https://doi.org/10.1038/nature15541
  23. He WT, Wan H, Hu L, Chen P, Wang X, Huang Z, Yang ZH, Zhong CQ, Han J. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res 2015;25:1285-1298. https://doi.org/10.1038/cr.2015.139
  24. Jeong SJ, Kim S, Park JG, Jung IH, Lee MN, Jeon S, Kweon HY, Yu DY, Lee SH, Jang Y, et al. Prdx1 (peroxiredoxin 1) deficiency reduces cholesterol efflux via impaired macrophage lipophagic flux. Autophagy 2018;14:120-133. https://doi.org/10.1080/15548627.2017.1327942
  25. Jeong SJ, Cho MJ, Ko NY, Kim S, Jung IH, Min JK, Lee SH, Park JG, Oh GT. Deficiency of peroxiredoxin 2 exacerbates angiotensin II-induced abdominal aortic aneurysm. Exp Mol Med 2020;52:1587-1601. https://doi.org/10.1038/s12276-020-00498-3
  26. Wang Y, Zhao Y, Wang Z, Sun R, Zou B, Li R, Liu D, Lin M, Zhou J, Ning S, et al. Peroxiredoxin 3 inhibits acetaminophen-induced liver pyroptosis through the regulation of mitochondrial ROS. Front Immunol 2021;12:652782.
  27. Nabeshima A, Yamada S, Guo X, Tanimoto A, Wang KY, Shimajiri S, Kimura S, Tasaki T, Noguchi H, Kitada S, et al. Peroxiredoxin 4 protects against nonalcoholic steatohepatitis and type 2 diabetes in a nongenetic mouse model. Antioxid Redox Signal 2013;19:1983-1998. https://doi.org/10.1089/ars.2012.4946
  28. Kim MH, Seong JB, Huh JW, Bae YC, Lee HS, Lee DS. Peroxiredoxin 5 ameliorates obesity-induced nonalcoholic fatty liver disease through the regulation of oxidative stress and AMP-activated protein kinase signaling. Redox Biol 2020;28:101315.
  29. Roh JS, Sohn DH. Damage-associated molecular patterns in inflammatory diseases. Immune Netw 2018;18:e27.
  30. Gim E, Shim DW, Hwang I, Shin OS, Yu JW. Zika virus impairs host NLRP3-mediated inflammasome activation in an NS3-dependent manner. Immune Netw 2019;19:e40.
  31. Kishore U, Gaboriaud C, Waters P, Shrive AK, Greenhough TJ, Reid KB, Sim RB, Arlaud GJ. C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol 2004;25:551-561. https://doi.org/10.1016/j.it.2004.08.006
  32. Wang Q, Rozelle AL, Lepus CM, Scanzello CR, Song JJ, Larsen DM, Crish JF, Bebek G, Ritter SY, Lindstrom TM, et al. Identification of a central role for complement in osteoarthritis. Nat Med 2011;17:1674-1679. https://doi.org/10.1038/nm.2543
  33. Bohana-Kashtan O, Ziporen L, Donin N, Kraus S, Fishelson Z. Cell signals transduced by complement. Mol Immunol 2004;41:583-597. https://doi.org/10.1016/j.molimm.2004.04.007
  34. Morgan BP. Complement membrane attack on nucleated cells: resistance, recovery and non-lethal effects. Biochem J 1989;264:1-14. https://doi.org/10.1042/bj2640001
  35. Stahl RA, Adler S, Baker PJ, Chen YP, Pritzl PM, Couser WG. Enhanced glomerular prostaglandin formation in experimental membranous nephropathy. Kidney Int 1987;31:1126-1131. https://doi.org/10.1038/ki.1987.118
  36. Hansch GM, Seitz M, Betz M. Effect of the late complement components C5b-9 on human monocytes: release of prostanoids, oxygen radicals and of a factor inducing cell proliferation. Int Arch Allergy Appl Immunol 1987;82:317-320. https://doi.org/10.1159/000234216
  37. Ruparelia N, Chai JT, Fisher EA, Choudhury RP. Inflammatory processes in cardiovascular disease: a route to targeted therapies. Nat Rev Cardiol 2017;14:133-144. https://doi.org/10.1038/nrcardio.2016.185
  38. Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease--a double-edged sword. Neuron 2002;35:419-432. https://doi.org/10.1016/S0896-6273(02)00794-8
  39. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006;444:860-867. https://doi.org/10.1038/nature05485
  40. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-867. https://doi.org/10.1038/nature01322
  41. Guo H, Callaway JB, Ting JP. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 2015;21:677-687.  https://doi.org/10.1038/nm.3893