Advertisement

pp 1-9 | Cite as

Phagocytosis and Autophagy in THP-1 Cells Exposed to Urban Dust: Possible Role of LC3-Associated Phagocytosis and Canonical Autophagy

  • A. HolowniaEmail author
  • A. Niechoda
  • J. Lachowicz
  • E. Golabiewska
  • U. Baranowska
Chapter
Part of the Advances in Experimental Medicine and Biology book series

Abstract

Exposure to ambient particulate matter (PM) increases mortality and morbidity due to respiratory and cardiovascular diseases. The aim of this study was to assess the effect of standardized urban dust (UD) on phagocytosis and autophagy in a monocyte-macrophage cell line (THP-1 cells). The cells were grown for 24 h in the medium supplemented with 200 μg·mL−1 coarse carbon black (CB) or UD. In some experiments glutathione (GSH) was depleted in THP-1 cells by buthionine sulfoximine. The cells were double stained with green latex beads (phagocytosis) and with red autophagy marker (LC3) and were evaluated in a flow cytometer. In naïve THP-1 cells, about 61% of them were classified as “negative,” while 39% were classified as “double-positive.” Both GSH depletion and UD treatment produced three distinct subpopulations of cells on bivariate scatterplots. A new subpopulation of cells (about 24% of the total number) appeared, with a lower autophagy and phagocytosis, but with a higher autophagy/phagocytosis ratio, when compared to highly positive cells. CB affected, to some extent, phagocytosis without a substantial effect on autophagy. In conclusion, the research on distinct pathways of immune cell activation may be relevant to the diagnostics and therapy of PM-induced pneumotoxicity, inflammation, and tumorigenesis.

Keywords

Autophagy Carbon black Phagocytosis THP-1 cells Urban dust 

Notes

Conflicts of Interest

The authors had no conflicts of interest to declare in relation to this article.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Alexis NE, Lay JC, Zeman K, Bennett WE, Peden DB, Soukup JM, Devlin RB, Becker S (2006) Biological material on inhaled coarse fraction particulate matter activates airway phagocytes in vivo in healthy volunteers. J Allergy Clin Immunol 117:1396–1403Google Scholar
  2. Anderson JO, Thundiyil JG, Stolbach A (2012) Clearing the air: a review of the effects of particulate matter air pollution on human health. J Med Toxicol 8:166–175Google Scholar
  3. Baharom F, Rankin G, Blomberg A, Smed-Sörensen A (2017) Human lung mononuclear phagocytes in health and disease. Front Immunol 8:499Google Scholar
  4. Bai R, Guan L, Zhang W, Xu J, Rui W, Zhang F, Ding W (2016) Comparative study of the effects of PM1-induced oxidative stress on autophagy and surfactant protein B and C expressions in lung alveolar type II epithelial MLE-12 cells. Biochim Biophys Acta 1860:2782–2792Google Scholar
  5. Booth LA, Tavallai S, Hamed HA, Cruickshanks N, Denta P (2014) The role of cell signalling in the crosstalk between autophagy and apoptosis. Cell Signal 26:549–555Google Scholar
  6. Chen Y, Klionsky DJ (2011) The regulation of autophagy – unanswered questions. J Cell Sci 124:161–170Google Scholar
  7. Dale DC, Boxer L, Liles WC (2008) The phagocytes: neutrophils and monocytes. Blood 112:935–945Google Scholar
  8. de Oliveira Alves N, Matos Loureiro AL, Dos Santos FC, Nascimento KH, Dallacort R, de Castro Vasconcellos P, de Souza Hacon S, Artaxo P, de Medeiros SR (2011) Genotoxicity and composition of particulate matter from biomass burning in the eastern Brazilian Amazon region. Ecotoxicol Environ Saf 74:1427–1433Google Scholar
  9. de Oliveira Alves N, de Souza Hacon S, de Oliveira Galvao MF, Simoes Peixotoc M, Artaxo P, de Castro Vasconcellos P, de Medeiros SR (2014) Genetic damage of organic matter in the Brazilian Amazon: a comparative study between intense and moderate biomass burning. Environ Res 130:51–58Google Scholar
  10. Dobrovolskaia MA, Aggarwal P, Hall JB, McNeil SE (2008) Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol Pharm 5:487–495Google Scholar
  11. Donaldson K, Stone V, Clouter A, Renwick L, MacNee W (2001) Ultrafine particles. Occup Environ Med 58:211–206Google Scholar
  12. Donaldson K, Stone V, Borm PJ, Jimenez LA, Gilmour PS, Schins RP, Knaapen AM, Rahman I, Faux SP, Brown DM, MacNee W (2003) Oxidative stress and calcium signaling in the adverse effects of environmental particles (PM10). Free Radic Biol Med 34:1369–1382Google Scholar
  13. Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, Mills N, MacNee W, Stone V (2005) Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol 2:10Google Scholar
  14. Grodzki AC, Giulivi C, Lein PJ (2013) Oxygen tension modulates differentiation and primary macrophage functions in the human monocytic THP-1 cell line. PLoS One 8:e54926Google Scholar
  15. Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012:948098Google Scholar
  16. Heckmann BL, Boada-Romero E, Cunha LD, Magne J, Green DR (2017) LC3-associated phagocytosis and inflammation. J Mol Biol 429:3561–3576Google Scholar
  17. Kalai Selvi S, Vinoth A, Varadharajan T, Weng CF, Vijaya Padma V (2017) Neferine augments therapeutic efficacy of cisplatin through ROS-mediated non-canonical autophagy in human lung adenocarcinoma (A549 cells). Food Chem Toxicol 103:28–40Google Scholar
  18. Lai CH, Lee CN, Bai KJ, Yang YL, Chuang KJ, Wu SM, Chuanga HC (2016) Protein oxidation and degradation caused by particulate matter. Sci Rep 6:33727Google Scholar
  19. Lawal AO (2017) Air particulate matter induced oxidative stress and inflammation in cardiovascular disease and atherosclerosis: the role of Nrf2 and AhR-mediated pathways. Toxicol Lett 270:88–95Google Scholar
  20. Li Z, Wu Y, Chen HP, Zhu C, Dong L, Wang Y, Liu H, Xu X, Zhou J, Wu Y, Li W, Ying S, Shen H, Chen ZH (2018) MTOR suppresses environmental particle-induced inflammatory response in macrophages. J Immunol 200:2826–2834Google Scholar
  21. Liu KK, Qiu WR, Naveen Raj E, Liu HF, Huang HS, Lin YW, Chang CJ, Chen TH, Chen C, Chang HC, Hwang JK, Chao JI (2017) Ubiquitin-coated nanodiamonds bind to autophagy receptors for entry into the selective autophagy pathway. Autophagy 13:187–200Google Scholar
  22. Mancilla H, Maldonado R, Cereceda K, Villarroel-Espíndola F, Montes de Oca M, Angulo C, Castro MA, Slebe JC, Vera JC, Lavandero S, Concha II (2015) Glutathione depletion induces spermatogonial cell autophagy. J Cell Biochem 116:2283–2292Google Scholar
  23. Mantovani A, Schioppa T, Biswas SK, Marchesi F, Allavena P, Sica A (2003) Tumor-associated macrophages and dendritic cells as prototypic type II polarized myeloid populations. Tumori 89:459–468Google Scholar
  24. Manzano-Leon N, Quintana R, Sanchez B, Serrano J, Vega E, Vazquez-Lopez I, Rojas-Bracho L, Lopez-Villegas T, O’Neill MS, Vadillo-Ortega F, De Vizcaya-Ruiz A, Rosas I, Osornio-Vargas AR (2013) Variation in the composition and in vitro proinflammatory effect of urban particulate matter from different sites. J Biochem Mol Toxicol 27:87–97Google Scholar
  25. Matsuzawa-Ishimoto Y, Hwang S, Cadwell K (2018) Autophagy and inflammation. Annu Rev Immunol 36:73–101Google Scholar
  26. Nicholas SA, Sumbayev VV (2009) The involvement of hypoxia-inducible factor-1 alpha in Toll-like receptor 7/8-mediated inflammatory response. Cell Res 19:973–983Google Scholar
  27. Park S, Seok JK, Kwak JY, Suh HJ, Kim YM, Boo YC (2016) Anti-inflammatory effects of pomegranate peel extract in THP-1 cells exposed to particulate matter PM10. Evid Based Complement Alternat Med 2016:6836080Google Scholar
  28. Peixoto MS, de Oliveira Galvao MF, Batistuzzo de Medeiros SR (2017) Cell death pathways of particulate matter toxicity. Chemosphere 188:32–48Google Scholar
  29. Sahu D, Kannan GM, Vijayaraghavan R (2014) Carbon black particle exhibits size dependent toxicity in human monocytes. Int J Inflamm 2014:827019Google Scholar
  30. Singh A, Kendall SL, Campanella M (2018) Common traits spark the mitophagy/xenophagy interplay. Front Physiol 9:1172Google Scholar
  31. Stoeger T, Reinhard C, Takenaka S, Schroeppel A, Karg E, Ritter B, Heyder J, Schulz H (2006) Instillation of six different ultrafine carbon particles indicates a surface area threshold dose for acute lung inflammation in mice. Environ Health Perspect 114:328–333Google Scholar
  32. Szabó-Taylor KÉ, Tóth EÁ, Balogh AM, Sódar BW, Kádár L, Pálóczi K, Fekete N, Németh A, Osteikoetxea X, Vukman KV, Holub M, Pállinger É, Nagy G, Winyard PG, Buzás EI (2017) Monocyte activation drives preservation of membrane thiols by promoting release of oxidised membrane moieties via extracellular vesicles. Free Radic Biol Med 108:56–65Google Scholar
  33. Yamawaki H, Iwai N (2006) Mechanisms underlying nano-sized air-pollution-mediated progression of atherosclerosis: carbon black causes cytotoxic injury/inflammation and inhibits cell growth in vascular endothelial cells. Circ J 70:129–140Google Scholar
  34. Zhang Y, Morgan MJ, Chen K, Choksi S, Liu ZG (2012) Induction of autophagy is essential for monocyte-macrophage differentiation. Blood 119:2895–2905Google Scholar
  35. Zhao J, Riediker M (2014) Detecting the oxidative reactivity of nanoparticles: a new protocol for reducing artifacts. J Nanopart Res 16:2493Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • A. Holownia
    • 1
    Email author
  • A. Niechoda
    • 1
  • J. Lachowicz
    • 1
  • E. Golabiewska
    • 1
  • U. Baranowska
    • 1
  1. 1.Department of PharmacologyMedical UniversityBialystokPoland

Personalised recommendations