Systems Biology Reveals Cigarette Smoke-Induced Concentration-Dependent Direct and Indirect Mechanisms That Promote Monocyte-Endothelial Cell Adhesion

Toxicological Sciences

Volumn 147, Issue 2, 2015, Pages 370-385

  Poussin, Carine ^a   Laurent, Alexandra ^a   Peitsch, Manuel C ^a   Hoeng, Julia ^a   De Leon, Hector ^a  

^a PHILIP MORRIS PRODUCTS S A   (Switzerland)

Author keywords

Adhesion; Atherosclerosis; Cigarette smoke; Endothelial cell; Monocyte; Systems biology

Indexed keywords

CELL ADHESION MOLECULE; CIGARETTE SMOKE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FRACTALKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 2; VASCULAR CELL ADHESION MOLECULE 1;

ANTIGEN PRESENTATION; ARTICLE; CELL ADHESION; CELL DEATH; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CELL STRESS; CELL SURFACE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA DAMAGE; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MEDIATOR RELEASE; MONOCYTE; PROTEIN CONTENT; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TRANSCRIPTOMICS; VASCULITIS; XENOBIOTIC METABOLISM; ADVERSE EFFECTS; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION PROFILING; METABOLISM; SMOKING; VASCULAR ENDOTHELIUM;

CELL ADHESION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION PROFILING; HUMANS; IN VITRO TECHNIQUES; MONOCYTES; NF-KAPPA B; SMOKING; SYSTEMS BIOLOGY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84943736778     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv137     Document Type: Article

References (65)

1. Adams, M. R., Jessup, W., and Celermajer, D. S. (1997). Cigarette smoking is associated with increased human monocyte adhesion to endothelial cells: reversibility with oral L-arginine but not vitamin C. J. Am. Coll. Cardiol. 29, 491-497.
2. Arimilli, S., Damratoski, B. E., Bombick, B., Borgerding, M. F., and Prasad, G. L. (2012). Evaluation of cytotoxicity of different tobacco product preparations. Regul. Toxicol. Pharmacol. 64, 350-360.
3. Armstrong, L., Godinho, S. I., Uppington, K. M., Whittington, H. A., and Millar, A. B. (2006). Contribution of TNF-alpha converting enzyme and proteinase-3 to TNF-alpha processing in human alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 34, 219-225.
4. Armstrong, L., Godinho, S. I., Uppington, K. M., Whittington, H. A., and Millar, A. B. (2009). Tumour necrosis factoralpha processing in interstitial lung disease: a potential role for exogenous proteinase-3. Clin. Exp. Immunol. 156, 336-343.
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Series B 57, 289-300.
6. Black, R. A., Rauch, C. T., Kozlosky, C. J., Peschon, J. J., Slack, J. L., Wolfson, M. F., Castner, B. J., Stocking, K. L., Reddy, P., Srinivasan, S., et al. (1997). A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733.
7. Bodenhofer, U., Kothmeier, A., and Hochreiter, S. (2011). APCluster: an R package for affinity propagation clustering. Bioinformatics 27, 2463-2464.
8. Bradley, J. R., Johnson, D. R., and Pober, J. S. (1993). Endothelial activation by hydrogen peroxide. Selective increases of intercellular adhesion molecule-1 and major histocompatibility complex class I. Am. J. Pathol. 142, 1598-1609.
9. Collins, T., Lapierre, L. A., Fiers, W., Strominger, J. L., and Pober, J. S. (1986). Recombinant human tumor necrosis factor increases mRNA levels and surface expression of HLA-A, B antigens in vascular endothelial cells and dermal fibroblasts in vitro. Proc. Natl. Acad. Sci. USA 83, 446-450.
10. Csordas, A., Kreutmayer, S., Ploner, C., Braun, P. R., Karlas, A., Backovic, A., Wick, G., and Bernhard, D. (2011). Cigarette smoke extract induces prolonged endoplasmic reticulum stress and autophagic cell death in human umbilical vein endothelial cells. Cardiovasc. Res. 92, 141-148.
11. Cumming, G., Fidler, F., and Vaux, D. L. (2007). Error bars in experimental biology. J. Cell Biol. 177, 7-11.
12. Damico, R., Simms, T., Kim, B. S., Tekeste, Z., Amankwan, H., Damarla, M., and Hassoun, P. M. (2011). p53 mediates cigarette smoke-induced apoptosis of pulmonary endothelial cells: inhibitory effects of macrophage migration inhibitor factor. Am. J. Respir. Cell Mol. Biol. 44, 323-332.
13. Erl, W., Weber, C., Wardemann, C., and Weber, P. C. (1995). Adhesion properties of Mono Mac 6, a monocytic cell line with characteristics of mature human monocytes. Atherosclerosis 113, 99-107.
14. Favero, G., Paganelli, C., Buffoli, B., Rodella, L. F., and Rezzani, R. (2014). Endothelium and its alterations in cardiovascular diseases: life style intervention. BioMed Res. Int. 801896.
15. Frey, B. J., and Dueck, D. (2007). Clustering by passing messages between data points. Science 315, 972-976.
16. Frohlich, M., Sund, M., Lowel, H., Imhof, A., Hoffmeister, A., and Koenig, W. (2003). Independent association of various smoking characteristics with markers of systemic inflammation in men. Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). Eur. Heart J. 24, 1365-1372.
17. Giunzioni, I., Bonomo, A., Bishop, E., Castiglioni, S., Corsini, A., and Bellosta, S. (2014). Cigarette smoke condensate affects monocyte interaction with endothelium. Atherosclerosis 234, 383-390.
18. Hermida, L., Poussin, C., Stadler, M. B., Gubian, S., Sewer, A., Gaidatzis, D., Hotz, H. R., Martin, F., Belcastro, V., Cano, S., et al. (2013). Confero: an integrated contrast data and gene set platform for computational analysis and biological interpretation of omics data. BMC Genomics 14, 514.
19. Hochreiter-Hufford, A., and Ravichandran, K. S. (2013). Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harbor Perspect. Biol. 5, a008748.
20. Hoeng, J., Talikka, M., Martin, F., Sewer, A., Yang, X., Iskandar, A., Schlage, W. K., and Peitsch, M. C. (2014). Case study: the role of mechanistic network models in systems toxicology. Drug Discov. Today 19, 183-192.
21. Howard, G., Wagenknecht, L. E., Burke, G. L., Diez-Roux, A., Evans, G. W., McGovern, P., Nieto, F. J., and Tell, G. S. (1998). Cigarette smoking and progression of atherosclerosis: The Atherosclerosis Risk in Communities (ARIC) Study. JAMA 279, 119-124.
22. Kalra, V. K., Ying, Y., Deemer, K., Natarajan, R., Nadler, J. L., and Coates, T. D. (1994). Mechanism of cigarette smoke condensate induced adhesion of human monocytes to cultured endothelial cells. J. Cell Physiol. 160, 154-162.
23. Kogel, U., Schlage, W. K., Martin, F., Xiang, Y., Ansari, S., Leroy, P., Vanscheeuwijck, P., Gebel, S., Buettner, A., Wyss, C., et al. (2014). A 28-day rat inhalation study with an integrated molecular toxicology endpoint demonstrates reduced exposure effects for a prototypic modified risk tobacco product compared with conventional cigarettes. Food Chem. Toxicol. 68, 204-217.
24. Lehr, H. A. (1993). Adhesion-promoting effects of cigarette smoke on leukocytes and endothelial cells. Ann. N Y Acad. Sci. 686, 112-118.
25. Lehr, H. A., Frei, B., and Arfors, K. E. (1994). Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo. Proc. Natl. Acad. Sci. USA 91, 7688-7692.
26. Lehr, H. A., Kress, E., Menger, M. D., Friedl, H. P., Hubner, C., Arfors, K. E., and Messmer, K. (1993). Cigarette smoke elicits leukocyte adhesion to endothelium in hamsters: inhibition by CuZn-SOD. Free Radic. Biol. Med. 14, 573-581.
27. Loukili, N., Rosenblatt-Velin, N., Rolli, J., Levrand, S., Feihl, F., Waeber, B., Pacher, P., and Liaudet, L. (2010). Oxidants positively or negatively regulate nuclear factor kappaB in a context-dependent manner. J. Biol. Chem. 285, 15746-15752. 10.1074/jbc. M110.103259.
28. Martin, F., Sewer, A., Talikka, M., Xiang, Y., Hoeng, J., and Peitsch, M. C. (2014). Quantification of biological network perturbations for mechanistic insight and diagnostics using two-layer causal models. BMC Bioinformatics 15, 238.
29. Messner, B., and Bernhard, D. (2014). Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arterioscler Thromb. Vasc. Biol. 34, 509-515.
30. Messner, B., Frotschnig, S., Steinacher-Nigisch, A., Winter, B., Eichmair, E., Gebetsberger, J., Schwaiger, S., Ploner, C., Laufer, G., and Bernhard, D. (2012). Apoptosis and necrosis: two different outcomes of cigarette smoke condensate-induced endothelial cell death. Cell Death Dis. 3, e424.
31. Moffatt, O. D., Devitt, A., Bell, E. D., Simmons, D. L., and Gregory, C. D. (1999). Macrophage recognition of ICAM-3 on apoptotic leukocytes. J. Immunol. 162, 6800-6810.
32. Muller, T. (1995). Expression of c-fos in quiescent Swiss 3T3 cells exposed to aqueous cigarette smoke fractions. Cancer Res. 55, 1927-1932.
33. Muller, T., and Gebel, S. (1994). Heme oxygenase expression in Swiss 3T3 cells following exposure to aqueous cigarette smoke fractions. Carcinogenesis 15, 67-72.
34. Nordskog, B. K., Blixt, A. D., Morgan, W. T., Fields, W. R., and Hellmann, G. M. (2003). Matrix-degrading and proinflammatory changes in human vascular endothelial cells exposed to cigarette smoke condensate. Cardiovasc. Toxicol. 3, 101-117.
35. Ouyang, Y., Virasch, N., Hao, P., Aubrey, M. T., Mukerjee, N., Bierer, B. E., and Freed, B. M. (2000). Suppression of human IL- 1beta, IL-2, IFN-gamma, and TNF-alpha production by cigarette smoke extracts. The J. Allergy Clin. Immunol. 106, 280-287.
36. Perna, A. F., Sepe, I., Lanza, D., Capasso, R., Zappavigna, S., Capasso, G., Caraglia, M., and Ingrosso, D. (2013). Hydrogen sulfide reduces cell adhesion and relevant inflammatory triggering by preventing ADAM17-dependent TNF-alpha activation. J. Cell Biochem. 114, 1536-1548.
37. Poussin, C., Gallitz, I., Schlage, W. K., Steffen, Y., Stolle, K., Lebrun, S., Hoeng, J., Peitsch, M. C., and Lietz, M. (2014). Mechanism of an indirect effect of aqueous cigarette smoke extract on the adhesion of monocytic cells to endothelial cells in an in vitro assay revealed by transcriptomics analysis. Toxicol. in vitro 28, 896-908.
38. Poussin, C., Ibberson, M., Hall, D., Ding, J., Soto, J., Abel, E. D., and Thorens, B. (2011). Oxidative phosphorylation flexibility in the liver of mice resistant to high-fat diet-induced hepatic steatosis. Diabetes 60, 2216-2224.
39. Rius, C., Company, C., Piqueras, L., Cerda-Nicolas, J. M., Gonzalez, C., Servera, E., Ludwig, A., Morcillo, E. J., and Sanz, M. J. (2013). Critical role of fractalkine (CX3CL1) in cigarette smoke-induced mononuclear cell adhesion to the arterial endothelium. Thorax 68, 177-186.
40. sbv IMPROVER project team, Ansari, S., Binder, J., Boue, S., Di Fabio, A., Hayes, W., Hoeng, J., Iskandar, A., Kleiman, R., Norel, R., et al (2013). On Crowd-verification of Biological Networks. Bioinformatics Biol. Insights 7, 307-325.
41. Schlage, W. K., Iskandar, A. R., Kostadinova, R., Xiang, Y., Sewer, A., Majeed, S., Kuehn, D., Frentzel, S., Talikka, M., Geertz, M., et al. (2014). In vitro systems toxicology approach to investigate the effects of repeated cigarette smoke exposure on human buccal and gingival organotypic epithelial tissue cultures. Toxicol. Mech. Methods 24, 470-487.
42. Scott, A. J., O'Dea, K. P., O'Callaghan, D., Williams, L., Dokpesi, J. O., Tatton, L., Handy, J. M., Hogg, P. J., and Takata, M. (2011). Reactive oxygen species and p38 mitogen-activated protein kinase mediate tumor necrosis factor alpha-converting enzyme (TACE/ADAM-17) activation in primary human monocytes. J. Biol. Chem. 286, 35466-35476.
43. Shao, M. X., Nakanaga, T., and Nadel, J. A. (2004). Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-alpha-converting enzyme in human airway epithelial (NCI-H292) cells. Am. J. Physiol. 287, L420-L427.
44. Sluiter, W., Pietersma, A., Lamers, J. M., and Koster, J. F. (1993). Leukocyte adhesion molecules on the vascular endothelium: their role in the pathogenesis of cardiovascular disease and the mechanisms underlying their expression. J. Cardiovasc. Pharmacol. 22(Suppl. 4), S37-S44.
45. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3(Article 3).
46. Su, Y., Han, W., Giraldo, C., De Li, Y., and Block, E. R. (1998). Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells. Am. J. Respir. Cell Mol. Biol. 19, 819-825.
47. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550.
48. Szczepanski, M., Kamianowska, M., and Kamianowski, G. (2012). Effects of fluorides on apoptosis and activation of human umbilical vein endothelial cells. Oral Dis. 18, 280-284.
49. Talikka, M., Kostadinova, R., Xiang, Y., Mathis, C., Sewer, A., Majeed, S., Kuehn, D., Frentzel, S., Merg, C., Geertz, M., et al. (2014). The response of human nasal and bronchial organotypic tissue cultures to repeated whole cigarette smoke exposure. Int. J. Toxicol. 33, 506-517.
50. Thomson, T. M., Sewer, A., Martin, F., Belcastro, V., Frushour, B. P., Gebel, S., Park, J., Schlage, W. K., Talikka, M., Vasilyev, D. M., et al. (2013). Quantitative assessment of biological impact using transcriptomic data and mechanistic network models. Toxicol. Appl. Pharmacol. 272, 863-878.
51. Tollefson, A. K., Oberley-Deegan, R. E., Butterfield, K. T., Nicks, M. E., Weaver, M. R., Remigio, L. K., Decsesznak, J., Chu, H. W., Bratton, D. L., Riches, D. W., et al. (2010). Endogenous enzymes (NOX and ECSOD) regulate smoke-induced oxidative stress. Free Radic. Biol. Med. 49, 1937-1946.
52. Walters, M. J., Paul-Clark, M. J., McMaster, S. K., Ito, K., Adcock, I. M., and Mitchell, J. A. (2005). Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance. Mol. Pharmacol. 68, 1343-1353.
53. Wang, Y., Wang, L., Ai, X., Zhao, J., Hao, X., Lu, Y., and Qiao, Z. (2004). Nicotine could augment adhesion molecule expression in human endothelial cells through macrophages secreting TNF-alpha, IL-1beta. Int. Immunopharmacol. 4, 1675-1686.
54. Weber, C., Erl, W., Weber, K., and Weber, P. C. (1996). Increased adhesiveness of isolated monocytes to endothelium is prevented by vitamin C intake in smokers. Circulation 93, 1488-1492.
55. Weissmuller, S., Semmler, L. Y., Kalinke, U., Christians, S., Muller-Berghaus, J., and Waibler, Z. (2012). ICOS-LICOS interaction is critically involved in TGN1412-mediated T-cell activation. Blood 119, 6268-6277.
56. Westerheide, S. D., and Morimoto, R. I. (2005). Heat shock response modulators as therapeutic tools for diseases of protein conformation. J. Biol. Chem. 280, 33097-33100.
57. Wheway, J., Obeid, S., Couraud, P. O., Combes, V., and Grau, G. E. (2013). The brain microvascular endothelium supports T cell proliferation and has potential for alloantigen presentation. PloS One 8, e52586.
58. Wright, W. R., Parzych, K., Crawford, D., Mein, C., Mitchell, J. A., and Paul-Clark, M. J. (2012). Inflammatory transcriptome profiling of human monocytes exposed acutely to cigarette smoke. PloS One 7, e30120.
59. Wu, Z., Irizarry, R. A., Gentleman, R., Murillo, F. M., and Spencer, F. (2004). A Model Based Background Adjustment for Oligonucleotide Expression Arrays. Johns Hopkins University, Department of Biostatistics Working Papers Working Paper 1.
60. Xu, L., Li, Z. L., Zhu, X. X., Ma, J., Hong, C. J., He, J. X., Xiang, D. C., and Qiu, J. (2009). [Expression of ICOSL on human coronary artery endothelial cells and its being interferentialed by ox- LDL]. Xi bao yu fen zi mian yi xue za zhi = Chin. J. Cell. Mol. Immunol. 25, 819-821.
61. Yanbaeva, D. G., Dentener, M. A., Creutzberg, E. C., Wesseling, G., and Wouters, E. F. (2007). Systemic effects of smoking. Chest 131, 1557-1566.
62. Yong, T., Zheng, M. Q., and Linthicum, D. S. (1997). Nicotine induces leukocyte rolling and adhesion in the cerebral microcirculation of the mouse. J. Neuroimmunol. 80, 158-164.
63. Zahler, S., Kupatt, C., and Becker, B. F. (2000). Endothelial preconditioning by transient oxidative stress reduces inflammatory responses of cultured endothelial cells to TNF-alpha. FASEB J. 14, 555-564.
64. Zapolska-Downar, D., Naruszewicz, M., Zapolski-Downar, A., Markiewski, M., Bukowska, H., and Millo, B. (2000). Ibuprofen inhibits adhesiveness of monocytes to endothelium and reduces cellular oxidative stress in smokers and non-smokers. Eur. J. Clin. Invest. 30, 1002-1010.
65. Zhang, X., Wang, L., Zhang, H., Guo, D., Zhao, J., Qiao, Z., and Qiao, J. (2002). The effects of cigarette smoke extract on the endothelial production of soluble intercellular adhesion molecule- 1 are mediated through macrophages, possibly by inducing TNF-alpha release. Methods Find Exp. Clin. Pharmacol. 24, 261-265.