Abstract
Low-density lipoprotein (LDL) was recently reported to be an opsonin, enhancing the phagocytosis of group A Streptococcus (GAS) by human monocytic leukemia U937 cells due to the binding of LDL to some GAS strains. We postulated that LDL might also promote the opsonophagocytosis of Pseudomonas aeruginosa by U937 cells since this bacterium interacts with LDL. In this study, P. aeruginosa (CMCC10104), U937 cells, and human LDL were used in phagocytosis assays to test our hypothesis. Escherichia coli strain BL21, which does not interact with LDL, was used as a negative control. Colony counting and fluorescence microscopy were used to determine the bacterial quantity in the opsonophagocytosis assays. After incubation of U937 cells and P. aeruginosa with LDL (100 µg/ml) for 15 and 30 min, phagocytosis was observed to be increased by 22.71% and 32.90%, respectively, compared to that seen in the LDL-free group. However, LDL did not increase the phagocytosis of E. coli by U937 cells. In addition, we identified CD36 as a major opsonin receptor on U937 cells, since an anti-CD36 monoclonal antibody, but not an anti-CD4 monoclonal antibody, almost completely abolished the opsonophagocytosis of P. aeruginosa by U937 cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bambauer, R., Bambauer, C., Lehmann, B., Latza, R., and Schiel, R. 2012. LDL-apheresis: technical and clinical aspects. Scientific-World Journal 2012, 314283.
Berne, S., Lah, L., and Sepcić, K. 2010. Aegerolysins: structure, function, and putative biological role. Protein Sci. 18, 694–706.
Choromańska, B., Myśliwiec, P., Choromańska K., Dadan, J., and Chabowski, A. 2017. The role of CD36 receptor in the pathogenesis of atherosclerosis. Adv. Clin. Exp. Med. 26, 717–722.
Han, R. 2010. Plasma lipoproteins are important components of the immune system. Microbiol. Immunol. 54, 246–253.
Kim, J.B., Xia, Y.R., Romanoski, C.E., Lee, S., Meng, Y., Shi, Y.S., Bourquard, N., Gong, K.W., Port, Z., Grijalva, V., et al. 2011. Paraoxonase-2 modulates stress response of endothelial cells to oxidized phospholipids and a bacterial quorum-sensing molecule. Arterioscler. Thromb. Vasc. Biol. 31, 2624–2633.
Kinoshita, M., Kato, H., Yasumoto, H., Shimizu, M., Hamaoka, S., Naito, Y., Akiyama, K., Moriyama, K., and Sawa, T. 2016. The prophylactic effects of human IgG derived from sera containing high anti-PcrV titers against pneumonia-causing Pseudomonas aeruginosa. Hum. Vaccin. Immunother. 12, 2833–2846.
Levi, M., van der Poll, T., and Schultz, M. 2012. Infection and inflammation as risk factors for thrombosis and atherosclerosis. Semin. Thromb. Hemost. 38, 506–514.
Liu, L., Zhou, L., Li, Y., Bai, W., Liu, N., Li, W., Gao, Y., Liu, Z., and Han, R. 2015. High-density lipoprotein acts as an opsonin to enhance phagocytosis of group A Streptococcus by U937 cells. Microbiol. Immunol. 59, 419–425.
Lovewell, R.R., Patankar, Y.R., and Berwin, B. 2014. Mechanisms of phagocytosis and host clearance of Pseudomonas aeruginosa. Am. J. Physiol. Lung Cell. Mol. Physiol. 306, L591–603.
Luangrath, V., Brodeur, M.R., Rhainds, D., and Brissette, L. 2008. Mouse CD36 has opposite effects on LDL and oxidized LDL metabolism in vivo. Arterioscler. Thromb. Vasc. Biol. 28, 1290–1295.
Makoveichuk, E., Cherepanov, P., Lundberg, S., Forsberg, A., and Olivecrona, G. 2003. pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid Res. 44, 320–330.
Mclaren, D.G., Wang, S.P., Stout, S.J., Xie, D., Miller, P.L., Mendoza, V., Rosa, R., Castroperez, J., Previs, S.F., and Johns, D.G. 2013. Tracking fatty acid kinetics in distinct lipoprotein fractions in vivo: a novel high-throughput approach for studying dyslipidemia in rodent models. J. Lipid Res. 54, 276–281.
Micek, S.T., Wunderink, R.G., Kollef, M.H., Chen, C., Rello, J., Chastre, J., Antonelli, M., Welte, T., Clair, B., Ostermann, H., et al. 2015. An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: impact of multidrug resistance. Crit. Care 19, 219.
Millares, L., Martí, S., Ardanuy, C., Liñares, J., Santos, S., Dorca, J., Garcíanuñez, M., Quero, S., and Monsó, E. 2017. Specific IgA against Pseudomonas aeruginosa in severe COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 12, 2807–2811.
Mulet, X., Moyá, B., Juan, C., Macià, M.D., Pérez, J.L., Blázquez, J., and Oliver, A. 2011. Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrob. Agents Chemother. 55, 4560–4568.
Pluddemann, A., Mukhopadhyay, S., and Gordon, S. 2006. The interaction of macrophage receptors with bacterial ligands. Expert Rev. Mol. Med. 8, 1–25.
Rao, J., DiGiandomenico, A., Unger, J., Bao, Y., Polanowska-Grabowska, R.K., and Goldberg, J.B. 2008. A novel oxidized lowdensity lipoprotein-binding protein from Pseudomonas aeruginosa. Microbiology 154, 654–665.
Ravnskov, U. and McCully, K.S. 2012. Infections may be causal in the pathogenesis of atherosclerosis. Am. J. Med. Sci. 344, 391–394.
Safar, J.G., Wille, H., Geschwind, M.D., Deering, C., Latawiec, D., Serban, A., King, D.J., Legname, G., Weisgraber, K.H., and Mahley, R.W. 2006. Human prions and plasma lipoproteins. Proc. Natl. Acad. Sci. USA 103, 11312.
Silverstein, R.L. and Febbraio, M. 2009. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2, re3.
Zani, I.A., Stephen, S.L., Mughal, N.A., Russell, D., Homer-Vanniasinkam, S., Wheatcroft, S.B., and Ponnambalam, S. 2015. Scavenger receptor structure and function in health and disease. Cells 4, 178–201.
Zhou, L., Liu, L., Yang, J., Li, Y., Bai, W., Liu, N., Li, W., Gao, Y., Xu, L., and Liu, Z. 2016. LDL acts as an opsonin enhancing the phagocytosis of group A Streptococcus by monocyte and whole human blood. Med. Microbiol. Immunol. 205, 155–162.
Acknowledgements
The authors thank Ling Liu and En Liu for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, Y., Liu, Z., Yang, J. et al. Low-density lipoprotein as an opsonin promoting the phagocytosis of Pseudomonas aeruginosa by U937 cells. J Microbiol. 57, 711–716 (2019). https://doi.org/10.1007/s12275-019-8413-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-019-8413-3