Protective Effect of an Anti-HMGB-1 Neutralizing Antibody on Hemozoin-Induced Alveolar Epithelial Cell in a Model of Malaria Associated ALI/ARDS
-
Tachpon Techarang
,
Pitchanee Jariyapong
,
Parnpen Viriyavejakul
,
Supattra Glaharn
,
Charit Srisook
,
Chuchard Punsawad
Abstract
Background: We aimed to determine whether neutralizing high mobility group box-1 (HMGB-1) prevents the release of HMGB-1 and proinflammatory cytokines on hemozoin (Hz)-induced alveolar epithelial cell in a model of malaria associated ALI/ARDS.
Methods: This study was conducted in the Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand in 2020. Human pulmonary alveolar epithelial cells (HPAEpiCs) were exposed to medium alone or 20 µM Hz for 24 h and incubated with different concentrations (1, 5, and 10 µg/ml) of anti-HMGB-1 monoclonal antibody (mAb) for various times (0, 4, 12, 24, and 48 h). The levels of HMGB-1, TNF-α and IFN-γ in the supernatants were measured by ELISA. The mRNA expression of RAGE, TLR-2 and TLR-4 were analyzed by real-time PCR.
Results: The HPAEpiCs treated with 10 µg/ml anti-HMGB-1 mAb showed a significant reduction in HMGB-1 release into the supernatant compared with those treated with 1 and 5 µg/ml anti-HMGB-1 mAb. The levels of TNF-α and IFN-γ were significantly decreased in the supernatant of HPAEpiCs treated with 1, 5, and 10 µg/ml anti-HMGB-1 mAb for 4, 12, 24, and 48 h compared with those stimulated with Hz alone. The mRNA expression levels of RAGE, TLR-2, and TLR-4 were significantly decreased after 24 h of anti-HMGB-1 antibody treatment at all concentrations.
Conclusions: An anti-HMGB-1 antibody could be an effective agent for inhibiting the release of HMGB-1, TNF-α and IFN-γ. Furthermore, a neutralizing anti-HMGB-1 antibody could be applicable for the treatment of malaria-associated ALI/ARDS.
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15. Yang H, Wang H, Ju Z, et al. MD-2 is required for disulfide HMGB1–dependent TLR4 signaling. J Exp Med. 2015;212(1):5-14.
16. Magna M, Pisetsky DS. The role of HMGB1 in the pathogenesis of inflammatory and autoimmune diseases. Mol Med. 2014; 20(1): 138–146.
17. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17(1):1-14.
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19. Zaher TE, Miller EJ, Morrow DMP, et al. Hyperoxia-induced signal transduction pathways in pulmonary epithelial cells. Free Radic Biol Med. 2007;42(7):897-908.
20. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25(4):402-8.
21. Griffith JW, Sun T, McIntosh MT, et al. Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208-5220.
22. Bobade D, Khandare AV, Deval M, et al. Hemozoin-induced activation of human monocytes toward M2-like phenotype is partially reversed by antimalarial drugs-chloroquine and artemisinin. Microbiologyopen. 2019; 8(3):e00651-e00651.
23. Jaramillo M, Plante I, Ouellet N, et al. Hemozoin-inducible proinflammatory events in vivo: Potential role in malaria infection. J Immunol. 2004;172(5):3101-10.
24. Lu B, Wang H, Andersson U, et al. Regulation of HMGB1 release by inflammasomes. Protein Cell. 2013;4(3):163-167.
25. Yoshihara-Hirata C, Yamashiro K, Yamamoto T, et al. Anti-HMGB1 neutralizing antibody attenuates periodontal inflammation and bone resorption in a murine periodontitis model. Infect Immun. 2018;86(5):e00111-18.
26. Yang H, Ochani M, Li J, Qiang X, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci U S A. 2004; 101(1):296-301.
27. Gong Q, Xu JF, Yin H, et al. Protective effect of antagonist of high-mobility group box 1 on lipopolysaccharide-induced acute lung injury in mice. Scand J Immunol. 2009;69(1):29-35.
28. Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med. 2005;201(7):1135-1143.
29. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139-62.
30. Wang D, Liu K, Wake H, et al. Anti-high mobility group box-1 (HMGB1) antibody inhibits hemorrhage-induced brain injury and improved neurological deficits in rats. Sci Rep. 2017;7:46243.
31. Kokkola R, Andersson A, Mullins G, et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol. 2005;61(1):1-9.
32. Yang H, Liu H, Zeng Q, et al. Inhibition of HMGB1/RAGE-mediated endocytosis by HMGB1 antagonist box A, anti-HMGB1 antibodies, and cholinergic agonists suppresses inflammation. Mol Med. 2019; 25(1):13.
33. van Zoelen MAD, Yang H, Florquin S,et al. Role of toll-like receptors 2 and 4, and the receptor for advanced glycation end products in high-mobility group box 1-induced inflammation in vivo. Shock. 2009;31(3):280-4.
34. van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis. 2008;11(1):91-9.
2. Deroost K, Tyberghein A, Lays N, et al. Hemozoin induces lung inflammation and correlates with malaria-associated acute respiratory distress syndrome. Am J Respir Cell Mol Biol. 2013; 48(5):589-600.
3. Milner D, Factor R, Whitten R, et al. Pulmonary pathology in pediatric cerebral malaria. Hum Pathol. 2013;44(12):2719-26.
4. Maknitikul S, Luplertlop N, Grau GER, et al. Dysregulation of pulmonary endothelial protein C receptor and thrombomodulin in severe falciparum malaria-associated ARDS relevant to hemozoin. PloS One. 2017; 12(7):e0181674.
5. Maknitikul S, Luplertlop N, Chaisri U, et al. Featured article: Immunomodulatory effect of hemozoin on pneumocyte apoptosis via CARD9 pathway, a possibly retarding pulmonary resolution. Exp Biol Med (Maywood). 2018;243(5):395-407.
6. Ding J, Cui X, Liu Q. Emerging role of HMGB1 in lung diseases: Friend or foe. J Cell Mol Med. 2017;21(6):1046-1057.
7. Ying S, Jiang Z, He X, et al. Serum HMGB1 as a potential biomarker for patients with asbestos-related diseases. Dis Markers. 2017;2017:5756102.
8. Angeletti D, Kiwuwa MS, Byarugaba J, et al. Elevated levels of high-mobility group box-1 (HMGB1) in patients with severe or uncomplicated Plasmodium falciparum malaria. Am J Trop Med Hyg. 2013;88(4):733-5.
9. Alleva LM, Yang H, Tracey KJ, et al. High mobility group box 1 (HMGB1) protein: Possible amplification signal in the pathogenesis of falciparum malaria. Trans R Soc Trop Med Hyg. 2005;99(3):171-4.
10. Higgins SJ, Xing K, Kim H, et al. Systemic release of high mobility group box 1 (HMGB1) protein is associated with severe and fatal Plasmodium falciparum malaria. Malar J. 2013;12:105.
11. Lee S, Kwak M, Kim S, et al. The role of high mobility group box 1 in innate immunity. Yonsei Med J. 2014;55(5):1165-76.
12. Yang H, Wang H, Chavan SS, et al. High mobility group box protein 1 (HMGB1): The prototypical endogenous danger molecule. Mol Med. 2015;21 Suppl 1:S6-S12.
13. Mantell LL, Parrish WR, Ulloa L. HMGB-1 as a therapeutic target for infectious and inflammatory disorders. Shock. 2006; 25(1):4-11.
14. Sohun M, Shen H. The implication and potential applications of high-mobility group box 1 protein in breast cancer. Ann Transl Med. 2016; 4(11):217.
15. Yang H, Wang H, Ju Z, et al. MD-2 is required for disulfide HMGB1–dependent TLR4 signaling. J Exp Med. 2015;212(1):5-14.
16. Magna M, Pisetsky DS. The role of HMGB1 in the pathogenesis of inflammatory and autoimmune diseases. Mol Med. 2014; 20(1): 138–146.
17. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17(1):1-14.
18. Ueno H, Matsuda T, Hashimoto S, et al. Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med. 2004; 170(12):1310-6.
19. Zaher TE, Miller EJ, Morrow DMP, et al. Hyperoxia-induced signal transduction pathways in pulmonary epithelial cells. Free Radic Biol Med. 2007;42(7):897-908.
20. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25(4):402-8.
21. Griffith JW, Sun T, McIntosh MT, et al. Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208-5220.
22. Bobade D, Khandare AV, Deval M, et al. Hemozoin-induced activation of human monocytes toward M2-like phenotype is partially reversed by antimalarial drugs-chloroquine and artemisinin. Microbiologyopen. 2019; 8(3):e00651-e00651.
23. Jaramillo M, Plante I, Ouellet N, et al. Hemozoin-inducible proinflammatory events in vivo: Potential role in malaria infection. J Immunol. 2004;172(5):3101-10.
24. Lu B, Wang H, Andersson U, et al. Regulation of HMGB1 release by inflammasomes. Protein Cell. 2013;4(3):163-167.
25. Yoshihara-Hirata C, Yamashiro K, Yamamoto T, et al. Anti-HMGB1 neutralizing antibody attenuates periodontal inflammation and bone resorption in a murine periodontitis model. Infect Immun. 2018;86(5):e00111-18.
26. Yang H, Ochani M, Li J, Qiang X, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci U S A. 2004; 101(1):296-301.
27. Gong Q, Xu JF, Yin H, et al. Protective effect of antagonist of high-mobility group box 1 on lipopolysaccharide-induced acute lung injury in mice. Scand J Immunol. 2009;69(1):29-35.
28. Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med. 2005;201(7):1135-1143.
29. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139-62.
30. Wang D, Liu K, Wake H, et al. Anti-high mobility group box-1 (HMGB1) antibody inhibits hemorrhage-induced brain injury and improved neurological deficits in rats. Sci Rep. 2017;7:46243.
31. Kokkola R, Andersson A, Mullins G, et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol. 2005;61(1):1-9.
32. Yang H, Liu H, Zeng Q, et al. Inhibition of HMGB1/RAGE-mediated endocytosis by HMGB1 antagonist box A, anti-HMGB1 antibodies, and cholinergic agonists suppresses inflammation. Mol Med. 2019; 25(1):13.
33. van Zoelen MAD, Yang H, Florquin S,et al. Role of toll-like receptors 2 and 4, and the receptor for advanced glycation end products in high-mobility group box 1-induced inflammation in vivo. Shock. 2009;31(3):280-4.
34. van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis. 2008;11(1):91-9.
| Files | ||
| Issue | Vol 16 No 3 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i3.7089 | |
| Keywords | ||
| HMGB1 protein; Malaria Acute lung injury | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Techarang T, Jariyapong P, Viriyavejakul P, Glaharn S, Srisook C, Punsawad C. Protective Effect of an Anti-HMGB-1 Neutralizing Antibody on Hemozoin-Induced Alveolar Epithelial Cell in a Model of Malaria Associated ALI/ARDS. Iran J Parasitol. 2021;16(3):366-376.
