Fol. Biol. 2021, 67, 183-190

https://doi.org/10.14712/fb2021067050183

Over-expression of Apolipoprotein J Inhibits Cholesterol Crystal-Induced Inflammatory Responses via Suppressing NLRP3 Inflammasome Activation in THP-1 Macrophages

Y. Li1, Y.-Q. Song2, Y. Zhang2, T. Liu2, Qin Qin1

1Department of Cardiology, Tianjin Chest Hospital, Jinnan City, Tianjin Province, China
2Cardiovascular Institute, Tianjin Chest Hospital, Jinnan City, Tianjin Province, China

Received June 2021
Accepted December 2021

References

1. Cacciapaglia, F., Anelli, M. G., Rinaldi, A., Fornaro, M., Lopalco, G., Scioscia, C., Lapadula, G., Iannone, F. (2018) Lipids and atherogenic indices fluctuation in rheumatoid arthritis patients on long-term tocilizumab treatment. Mediators Inflamm. 18, ID 2453265.
2. Corrado, E., Rizzo, M., Coppola, G., Fattouch, K., Novo, G., Marturana, I., Ferrara, F., Novo, S. (2010) An update on the role of markers of inflammation in atherosclerosis. J. Atheroscler. Thromb. 17, 1-11. <https://doi.org/10.5551/jat.2600>
3. Chang, C, C., Chu, C. F., Wang, C. N., Wu, H. T., Bi, K. W., Pang, J. H., Huang, S. T. (2014) The anti-atherosclerotic effect of tanshinone IIA is associated with the inhibition of TNF-α-induced VCAM-1, ICAM-1 and CX3CL1 expression. Phytomedicine 21, 207-216. <https://doi.org/10.1016/j.phymed.2013.09.012>
4. Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K., Dockrell, D. H. (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5, e8668. <https://doi.org/10.1371/journal.pone.0008668>
5. de Silva, H. V., Harmony, J. A., Stuart, W. D., Gil, C. M., Robbins, J. (1990) Apolipoprotein J: structure and tissue distribution. Biochemistry 29, 5380-5389. <https://doi.org/10.1021/bi00474a025>
6. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., Abela, G. S., Franchi, L., Nuñez, G., Schnurr, M., Espevik, T., Lien, E., Fitzgerald, K. A., Rock, K. L., Moore, K. J., Wright, S. D., Hornung, V., Latz, E. (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361. <https://doi.org/10.1038/nature08938>
7. Gelissen, I. C., Hochgrebe, T., Wilson, M. R., Easterbrook- Smith, S. B., Jessup, W., Dean, R. T., Brown, A. J. (1998) Apolipoprotein J (clusterin) induces cholesterol export from macrophage-foam cells: a potential anti-atherogenic function? Biochem. J. 331 (Pt 1), 231-237. <https://doi.org/10.1042/bj3310231>
8. Gisterå, A., Hansson, G. K. (2017) The immunology of atherosclerosis. Nat. Rev. Nephrol. 13, 368-380 <https://doi.org/10.1038/nrneph.2017.51>
9. Han, Z., Wang, Z., Cheng, G., Liu, B., Li, P., Li, J., Wang, W., Yin, C., Zhang, W. (2012) Presence, localization, and origin of clusterin in normal human spermatozoa. J. Assist. Reprod. Genet. 29, 751-757. <https://doi.org/10.1007/s10815-012-9779-x>
10. Hansson, G. K., Hermansson, A. (2011) The immune system in atherosclerosis. Nat. Immunol. 12, 204-212. <https://doi.org/10.1038/ni.2001>
11. Harden, J. L., Johnson-Huang, L. M., Chamian, M. F., Lee, E., Pearce, T., Leonardi, C. L., Haider, A., Lowes, M. A., Krueger, J. G. (2015) Humanized anti-IFN-γ (HuZAF) in the treatment of psoriasis. J. Allergy Clin. Immunol. 135, 553-556. <https://doi.org/10.1016/j.jaci.2014.05.046>
12. Jenne, D. E., Lowin, B., Peitsch, M. C., Böttcher, A., Schmitz, G., Tschopp, J. (1991) Clusterin (complement lysis inhibitor) forms a high density lipoprotein complex with apolipoprotein A-I in human plasma. J. Biol. Chem. 266, 11030-11036. <https://doi.org/10.1016/S0021-9258(18)99123-4>
13. Katz, S. S., Shipley, G. G., Small, D. M. (1976) Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. J. Clin. Invest. 58, 200-211. <https://doi.org/10.1172/JCI108450>
14. Kim, H. J., Yoo, E. K., Kim, J. Y., Choi, Y. K., Lee, H. J., Kim, J. K., Jeoung, N. H., Lee, K. U., Park, I. S., Min, B. H., Park, K. G., Lee, C. H., Aronow, B. J., Sata, M., Lee, I. K. (2009) Protective role of clusterin/apolipoprotein J against neointimal hyperplasia via antiproliferative effect on vascular smooth muscle cells and cytoprotective effect on endothelial cells. Arterioscler. Thromb. Vasc. Biol. 29, 1558-1564. <https://doi.org/10.1161/ATVBAHA.109.190058>
15. Liu, G., Zhang, H., Hao, F., Hao, J., Pan, L., Zhao, Q., Wo, J. (2018) Clusterin reduces cold ischemia-reperfusion injury in heart transplantation through regulation of NF-kB signaling and Bax/Bcl-xL expression. Cell. Physiol. Biochem. 45, 1003-1012. <https://doi.org/10.1159/000487295>
16. Livak, K. J., Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔ C(T)) method. Methods 25, 402-408. <https://doi.org/10.1006/meth.2001.1262>
17. MRC/BHF Heart Protection Study Collaborative Group (1999) MRC/BHF Heart Protection Study of cholesterol-lowering therapy and of antioxidant vitamin supplementation in a wide range of patients at increased risk of coronary heart disease death: early safety and efficacy experience. Eur. Heart J. 20, 725-741.
18. Niyonzima, N., Bakke, S. S., Gregersen, I., Holm, S., Sandanger, Ø., Orrem, H. L., Sporsheim, B., Ryan, L., Kong, X. Y., Dahl, T. B., Skjelland, M., Sørensen, K. K., Rokstad, A. M., Yndestad, A., Latz, E., Gullestad, L., Andersen, G. Ø., Damås, J. K., Aukrust, P., Mollnes, T. E., Halvorsen, B., Espevik, T. (2020) Cholesterol crystals use complement to increase NLRP3 signaling pathways in coronary and carotid atherosclerosis. EBioMedicine 60, 102985. <https://doi.org/10.1016/j.ebiom.2020.102985>
19. Ordovas-Montanes, J. M., Ordovas, J. M. (2012) Cholesterol, inflammasomes, and atherogenesis. Curr. Cardiovasc. Risk Rep. 6, 45-52. <https://doi.org/10.1007/s12170-011-0212-2>
20. Ozaki, E., Campbell, M., Doyle, S. L. (2015) Targeting the NLRP3 inflammasome in chronic inflammatory diseases: current perspectives. J. Inflamm. Res. 8, 15-27.
21. Park, S., Mathis, K. W., Lee, I. K. (2014) The physiological roles of apolipoprotein J/clusterin in metabolic and cardiovascular diseases. Rev. Endocr. Metab. Disord. 15, 45-53. <https://doi.org/10.1007/s11154-013-9275-3>
22. Poulakou, M. V., Paraskevas, K. I., Wilson, M. R., Iliopoulos, D. C., Tsigris, C., Mikhailidis, D. P., Perrea, D. (2008) Apolipoprotein J and leptin levels in patients with coronary heart disease. In Vivo 22, 537-542.
23. Rajamäki, K., Lappalainen, J., Oörni, K., Välimäki, E., Matikainen, S., Kovanen, P. T., Eklund, K. K. (2010) Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One 5, e11765. <https://doi.org/10.1371/journal.pone.0011765>
24. Ridker, P. M., Libby, P., MacFadyen, J. G., Thuren, T., Ballantyne, C., Fonseca, F., Koenig, W., Shimokawa, H., Everett, B. M., Glynn, R. J. (2018) Modulation of the interleukin-6 signalling pathway and incidence rates of atherosclerotic events and all-cause mortality: analyses from the Canakinumab Anti-Inflammatory Thrombosis Outcomes Study (CANTOS). Eur. Heart J. 39, 3499-3507. <https://doi.org/10.1093/eurheartj/ehy310>
25. Riwanto, M., Rohrer, L., Roschitzki, B., Besler, C., Mocharla, P., Mueller, M., Perisa, D., Heinrich, K., Altwegg, L., von Eckardstein, A., Lüscher, T. F., Landmesser, U. (2013) Altered activation of endothelial anti- and proapoptotic pathways by high-density lipoprotein from patients with coronary artery disease: role of high-density lipoproteinproteome remodeling. Circulation 127, 891-904. <https://doi.org/10.1161/CIRCULATIONAHA.112.108753>
26. Staff, A. C., Ranheim, T., Khoury, J., Henriksen, T. (1999) Increased contents of phospholipids, cholesterol, and lipid peroxides in decidua basalis in women with preeclampsia. Am. J. Obstet. Gynecol. 180, 587-592. <https://doi.org/10.1016/S0002-9378(99)70259-0>
27. Strowig, T., Henao-Mejia, J., Elinav, E., Flavell, R. (2012) Inflammasomes in health and disease. Nature 481, 278-286. <https://doi.org/10.1038/nature10759>
28. Van Dijk, A., Vermond, R. A., Krijnen, P. A., Juffermans, L. J., Hahn, N. E., Makker, S. P., Aarden, E., Hack, L. A., Spreeuwenberg, M., van Rossum, B. C., Meischl, C., Paulus, W. J., Van Milligen, F. J., Niessen, H. W. (2010) Intravenous clusterin administration reduces myocardial infarct size in rats. Eur. J. Clin. Invest. 40, 893-902. <https://doi.org/10.1111/j.1365-2362.2010.02345.x>
29. Wang, L., Zhu, L., Duan, C., Li, L., Chen, G. (2020) Total saponin of Dioscorea collettii attenuates MSU crystal‑induced inflammation via inhibiting the activation of the NALP3 inflammasome and caspase‑1 in THP‑1 macrophages. Mol. Med. Rep. 21, 2466-2474.
30. Yanni, A. E., Agrogiannis, G., Gkekas, C., Perrea, D. (2014) Clusterin/Apolipoprotein J immunolocalization on carotid artery is affected by TNF-α, cigarette smoking and antiplatelet treatment. Lipids Health Dis. 13, 70. <https://doi.org/10.1186/1476-511X-13-70>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive