Biomarkers of chronic acrolein inhalation exposure in mice: Implications for tobacco product-induced toxicity

Toxicological Sciences

Volumn 158, Issue 2, 2017, Pages 263-274

  Conklin, Daniel J ^a,b   Malovichko, Marina V ^a,b   Zeller, Iris ^a,b   Das, Trinath P ^a,b   Krivokhizhina, Tatiana V ^a,b   Lynch, Blake H ^a,b   Lorkiewicz, Pawel ^a,b   Agarwal, Abhinav ^a,b   Wickramasinghe, Nalinie ^a,b   Haberzettl, Petra ^a,b   Sithu, Srinivas D ^a   Shah, Jasmit ^a   O'Toole, Timothy E ^a,b   Rai, Shesh N ^a   Bhatnagar, Aruni ^a,b   Srivastava, Sanjay ^a,b  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

Aldehydes; Cardiovascular disease; Endothelial progenitor cells; Oxidative stress; Pulmonary injury; Tobacco

Indexed keywords

ACROLEIN; BIOLOGICAL MARKER;

ANIMAL; C57BL MOUSE; CHEMISTRY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; EXPOSURE; INSULIN RESISTANCE; LEUKOCYTE; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; SMOKE; TOBACCO; URINE;

ACROLEIN; ANIMALS; BIOMARKERS; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; INHALATION EXPOSURE; INSULIN RESISTANCE; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; SMOKE; TOBACCO;

EID: 85028357285     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfx095     Document Type: Article

References (69)

1. Appelman, L. M., Hendriksen, C. F., and Feron, V. J. (1981). Repeated exposure to alpha-ethylacrolein vapour: Subacute toxicity study in rats. Toxicology 22, 79-87.
2. Arcavi, L., and Benowitz, N. L. (2004). Cigarette smoking and infection. Arch. Intern. Med. 164, 2206-2216.
3. Borchers, M. T., Wesselkamper, S., Wert, S. E., Shapiro, S. D., and Leikauf, G. D. (1999). Monocyte inflammation augments acrolein-induced Muc5ac expression in mouse lung. Am. J. Physiol. 277, L489-L497.
4. Borchers, M. T., Wesselkamper, S. C., Deshmukh, H., Beckman, E., Medvedovic, M., Sartor, M., and Leikauf, G. D. (2009). The role of T cells in the regulation of acrolein-induced pulmonary inflammation and epithelial-cell pathology. Res. Rep. Health Eff. Inst. 146, 5-29.
5. Boulanger, C. M., Scoazec, A., Ebrahimian, T., Henry, P., Mathieu, E., Tedgui, A., and Mallat, Z. (2001). Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 104, 2649-2652.
6. Conklin, D. J., Barski, O. A., Lesgards, J. F., Juvan, P., Rezen, T., Rozman, D., Prough, R. A., Vladykovskaya, E., Liu, S., Srivastava, S., et al. (2010). Acrolein consumption induces systemic dyslipidemia and lipoprotein modification. Toxicol. Appl. Pharmacol. 243, 1-12.
7. Conklin, D. J., Guo, Y., Jagatheesan, G., Kilfoil, P. J., Haberzettl, P., Hill, B. G., Baba, S. P., Guo, L., Wetzelberger, K., Obal, D., et al. (2015). Genetic deficiency of glutathione S-transferase P increases myocardial sensitivity to ischemia-reperfusion injury. Circ. Res. 117, 437-449.
8. Conklin, D. J., Haberzettl, P., Jagatheesan, G., Baba, S., Merchant, M. L., Prough, R. A., Williams, J. D., Prabhu, S. D., and Bhatnagar, A. (2015). Glutathione S-transferase P protects against cyclophosphamide-induced cardiotoxicity in mice. Toxicol. Appl. Pharmacol. 285, 136-148.
9. Conklin, D. J., Haberzettl, P., Jagatheesan, G., Kong, M., and Hoyle, G. W. (2016). Role of TRPA1 in acute cardiopulmonary toxicity of inhaled acrolein. Toxicol. Appl. Pharmacol. 324, 61-72.
10. Conklin, D. J., Haberzettl, P., Lesgards, J. F., Prough, R. A., Srivastava, S., and Bhatnagar, A. (2009). Increased sensitivity of glutathione S-transferase P-null mice to cyclophosphamide-induced urinary bladder toxicity. J. Pharmacol. Exp. Ther. 331, 456-469.
11. Conklin, D. J., Haberzettl, P., Prough, R. A., and Bhatnagar, A. (2009). Glutathione-S-transferase P protects against endothelial dysfunction induced by exposure to tobacco smoke. Am. J. Physiol. Heart Circ. Physiol. 296, H1586-H1597.
12. Conklin, D. J., Prough, R. A., Juvan, P., Rezen, T., Rozman, D., Haberzettl, P., Srivastava, S., and Bhatnagar, A. (2011). Acrolein-induced dyslipidemia and acute-phase response are independent of HMG-CoA reductase. Mol. Nutr. Food Res. 55, 1411-1422.
13. deBethizy, J. D., Borgerding, M. F., Doolittle, D. J., Robinson, J. H., McManus, K. T., Rahn, C. A., Davis, R. A., Burger, G. T., Hayes, J. R., Reynolds, JHt., et al. (1990). Chemical and biological studies of a cigarette that heats rather than burns tobacco. J. Clin. Pharmacol. 30, 755-763.
14. DeJarnett, N., Conklin, D. J., Riggs, D. W., Myers, J. A., O'Toole, T. E., Hamzeh, I., Wagner, S., Chugh, A., Ramos, K. S., Srivastava, S., et al. (2014). Acrolein exposure is associated with increased cardiovascular disease risk. J. Am. Heart Assoc. 3, e000934.
15. Destaillats, H., Spaulding, R. S., and Charles, M. J. (2002). Ambient air measurement of acrolein and other carbonyls at the Oakland-San Francisco Bay Bridge Toll Plaza. Environ. Sci. Technol. 36, 2227-2235.
16. Dong, J. Z., and Moldoveanu, S. C. (2004). Gas chromatographymass spectrometry of carbonyl compounds in cigarette mainstream smoke after derivatization with 2, 4-dinitrophenylhydrazine. J. Chromatogr. A 1027, 25-35.
17. Eliasson, B., Attvall, S., Taskinen, M. R., and Smith, U. (1994). The insulin resistance syndrome in smokers is related to smoking habits. Arterioscler. Thromb. 14, 1946-1950.
18. Facchini, F. S., Hollenbeck, C. B., Jeppesen, J., Chen, Y. D., and Reaven, G. M. (1992). Insulin resistance and cigarette smoking. Lancet 339, 1128-1130.
19. Fadini, G. P., Losordo, D., and Dimmeler, S. (2012). Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ. Res. 110, 624-637.
20. Feron, V. J., Til, H. P., de Vrijer, F., Woutersen, R. A., Cassee, F. R., and van Bladeren, P. J. (1991). Aldehydes: Occurrence, carcinogenic potential, mechanism of action and risk assessment. Mutat. Res. 259, 363-385.
21. Ghilarducci, D. P., and Tjeerdema, R. S. (1995). Fate and effects of acrolein. Rev. Environ. Contam. Toxicol. 144, 95-146.
22. Haberzettl, P., Lee, J., Duggineni, D., McCracken, J., Bolanowski, D., O'Toole, T. E., Bhatnagar, A., and Conklin, D. J. (2012). Exposure to ambient air fine particulate matter prevents VEGF-induced mobilization of endothelial progenitor cells from the bone marrow. Environ. Health Perspect. 120, 848-856.
23. Haberzettl, P., Vladykovskaya, E., Srivastava, S., and Bhatnagar, A. (2009). Role of endoplasmic reticulum stress in acroleininduced endothelial activation. Toxicol. Appl. Pharmacol. 234, 14-24.
24. Haussmann, H. J. (2012). Use of hazard indices for a theoretical evaluation of cigarette smoke composition. Chem. Res. Toxicol. 25, 794-810.
25. Hazari, M. S., Haykal-Coates, N., Winsett, D. W., Krantz, Q. T., King, C., Costa, D. L., and Farraj, A. K. (2011). TRPA1 and sympathetic activation contribute to increased risk of triggered cardiac arrhythmias in hypertensive rats exposed to diesel exhaust. Environ. Health Perspect. 119, 951-957.
26. Heiss, C., Amabile, N., Lee, A. C., Real, W. M., Schick, S. F., Lao, D., Wong, M. L., Jahn, S., Angeli, F. S., Minasi, P., et al. (2008). Brief secondhand smoke exposure depresses endothelial progenitor cells activity and endothelial function: Sustained vascular injury and blunted nitric oxide production. J. Am. Coll. Cardiol. 51, 1760-1771.
27. Hill, J. M., Zalos, G., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., and Finkel, T. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N. Engl. J. Med. 348, 593-600.
28. Johnson, J. D., Houchens, D. P., Kluwe, W. M., Craig, D. K., and Fisher, G. L. (1990). Effects of mainstream and environmental tobacco smoke on the immune system in animals and humans: A review. Crit. Rev. Toxicol. 20, 369-395.
29. Kassem, N. O., Daffa, R. M., Liles, S., Jackson, S. R., Kassem, N. O., Younis, M. A., Mehta, S., Chen, M., Jacob, P., III, Carmella, S. G., et al. (2014). Children's exposure to secondhand and thirdhand smoke carcinogens and toxicants in homes of hookah smokers. Nicotine Tob. Res. 16, 961-975.
30. Keith, R. J., Al Rifai, M., Carruba, C., De Jarnett, N., McEvoy, J. W., Bhatnagar, A., Blaha, M. J., and Defilippis, A. P. (2016). Tobacco use, insulin resistance, and risk of type 2 diabetes: Results from the multi-ethnic study of atherosclerosis. PLoS One 11, e0157592.
31. Keith, R. J., Haberzettl, P., Vladykovskaya, E., Hill, B. G., Kaiserova, K., Srivastava, S., Barski, O., and Bhatnagar, A. (2009). Aldose reductase decreases endoplasmic reticulum stress in ischemic hearts. Chem. Biol. Interact. 178, 242-249.
32. Kondo, T., Hayashi, M., Takeshita, K., Numaguchi, Y., Kobayashi, K., Iino, S., Inden, Y., and Murohara, T. (2004). Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler. Thromb. Vasc. Biol. 24, 1442-1447.
33. Kosmider, L., Sobczak, A., Fik, M., Knysak, J., Zaciera, M., Kurek, J., and Goniewicz, M. L. (2014). Carbonyl compounds in electronic cigarette vapors-effects of nicotine solvent and battery output voltage. Nicotine Tob. Res. 16, 1319-1326.
34. Lambert, C., Li, J., Jonscher, K., Yang, T. C., Reigan, P., Quintana, M., Harvey, J., and Freed, B. M. (2007). Acrolein inhibits cytokine gene expression by alkylating cysteine and arginine residues in the NF-kappaB1 DNA binding domain. J. Biol. Chem 282, 19666-19675.
35. Lambert, C., McCue, J., Portas, M., Ouyang, Y., Li, J., Rosano, T. G., Lazis, A., and Freed, B. M. (2005). Acrolein in cigarette smoke inhibits T-cell responses. J. Allergy Clin. Immunol. 116, 916-922.
36. Li, L., Hamilton, R. F., Jr., and Holian, A. (1999). Effect of acrolein on human alveolar macrophage NF-kappaB activity. Am. J. Physiol. 277, L550-L557.
37. Li, L., Hamilton, R. F., Jr., Taylor, D. E., and Holian, A. (1997). Acrolein-induced cell death in human alveolar macrophages. Toxicol. Appl. Pharmacol. 145, 331-339.
38. Li, L., and Holian, A. (1998). Acrolein: A respiratory toxin that suppresses pulmonary host defense. Rev. Environ. Health 13, 99-108.
39. Martin, E. M., Clapp, P. W., Rebuli, M. E., Pawlak, E. A., Glista-Baker, E., Benowitz, N. L., Fry, R. C., and Jaspers, I. (2016). Ecigarette use results in suppression of immune and inflammatory-response genes in nasal epithelial cells similar to cigarette smoke. Am. J. Physiol. Lung Cell Mol. Physiol. 311, L135-L144.
40. McAuley, T. R., Hopke, P. K., Zhao, J., and Babaian, S. (2012). Comparison of the effects of e-cigarette vapor and cigarette smoke on indoor air quality. Inhal. Toxicol. 24, 850-857.
41. Medicine, I. O. 2010. Secondhand Smoke Exposure and Cardiovascular Effects. The National Academies, Washington, D.C.
42. Mogel, I., Baumann, S., Bohme, A., Kohajda, T., von Bergen, M., Simon, J. C., and Lehmann, I. (2011). The aromatic volatile organic compounds toluene, benzene and styrene induce COX-2 and prostaglandins in human lung epithelial cells via oxidative stress and p38 MAPK activation. Toxicology 289, 28-37.
43. Nelson, T. J., and Boor, P. J. (1982). Allylamine cardiotoxicity-IV. Metabolism to acrolein by cardiovascular tissues. Biochem. Pharmacol. 31, 509-514.
44. O'Toole, T. E., Abplanalp, W., Li, X., Cooper, N., Conklin, D. J., Haberzettl, P., and Bhatnagar, A. (2014). Acrolein decreases endothelial cell migration and insulin sensitivity through induction of let-7a. Toxicol. Sci. 140, 271-282.
45. O'Toole, T. E., Zheng, Y. T., Hellmann, J., Conklin, D. J., Barski, O., and Bhatnagar, A. (2009). Acrolein activates matrix metalloproteinases by increasing reactive oxygen species in macrophages. Toxicol. Appl. Pharmacol. 236, 194-201.
46. Penn, A., Nath, R., Pan, J., Chen, L., Widmer, K., Henk, W., and Chung, F. L. (2001). 1, N(2)-propanodeoxyguanosine adduct formation in aortic DNA following inhalation of acrolein. Environ. Health Perspect. 109, 219-224.
47. Persson, P. G., Carlsson, S., Svanstrom, L., Ostenson, C. G., Efendic, S., and Grill, V. (2000). Cigarette smoking, oral moist snuffuse and glucose intolerance. J. Intern. Med. 248, 103-110.
48. Pope, C. A., III, Bhatnagar, A., McCracken, J. P., Abplanalp, W., Conklin, D. J., and O'Toole, T. (2016). Exposure to fine particulate air pollution is associated with endothelial injury and systemic inflammation. Circ. Res. 119, 1204-1214.
49. Sansbury, B. E., Cummins, T. D., Tang, Y., Hellmann, J., Holden, C. R., Harbeson, M. A., Chen, Y., Patel, R. P., Spite, M., Bhatnagar, A., et al. (2012). Overexpression of endothelial nitric oxide synthase prevents diet-induced obesity and regulates adipocyte phenotype. Circ. Res. 111, 1176-1189.
50. Shihadeh, A., Salman, R., Jaroudi, E., Saliba, N., Sepetdjian, E., Blank, M. D., Cobb, C. O., and Eissenberg, T. (2012). Does switching to a tobacco-free waterpipe product reduce toxicant intake? A crossover study comparing CO, NO, PAH, volatile aldehydes, "tar" and nicotine yields. Food Chem. Toxicol. 50, 1494-1498.
51. Simak, J., Gelderman, M. P., Yu, H., Wright, V., and Baird, A. E. (2006). Circulating endothelial microparticles in acute ischemic stroke: A link to severity, lesion volume and outcome. J. Thromb. Haemost. 4, 1296-1302.
52. Sithu, S. D., Srivastava, S., Conklin, D. J., O'Toole, T. E., Bhatnagar, A., and D'Souza, S. E. (2008). Platelet Sensitivity is Increased by Acrolein. FASEB J. 22, 897-896.
53. Sithu, S. D., Srivastava, S., Siddiqui, M. A., Vladykovskaya, E., Riggs, D. W., Conklin, D. J., Haberzettl, P., O'Toole, T. E., Bhatnagar, A., and D'Souza, S. E. (2010). Exposure to acrolein by inhalation causes platelet activation. Toxicol. Appl. Pharmacol. 248, 100-110.
54. Srivastava, S., Sithu, S. D., Vladykovskaya, E., Haberzettl, P., Hoetker, D. J., Siddiqui, M. A., Conklin, D. J., D'Souza, S. E., and Bhatnagar, A. (2011). Oral exposure to acrolein exacerbates atherosclerosis in apoE-null mice. Atherosclerosis 215, 301-308.
55. Srivastava, S., Vladykovskaya, E., Barski, O. A., Spite, M., Kaiserova, K., Petrash, J. M., Chung, S. S., Hunt, G., Dawn, B., and Bhatnagar, A. (2009). Aldose reductase protects against early atherosclerotic lesion formation in apolipoprotein E-null mice. Circ. Res. 105, 793-802.
56. Stanfill, S. B., Calafat, A. M., Brown, C. R., Polzin, G. M., Chiang, J. M., Watson, C. H., and Ashley, D. L. (2003). Concentrations of nine alkenylbenzenes, coumarin, piperonal and pulegone in Indian bidi cigarette tobacco. Food Chem. Toxicol. 41, 303-317.
57. Stepanov, I., Jensen, J., Hatsukami, D., and Hecht, S. S. (2008). New and traditional smokeless tobacco: Comparison of toxicant and carcinogen levels. Nicotine Tob. Res. 10, 1773-1782.
58. Thompson, L. C., Ledbetter, A. D., Haykal-Coates, N., Cascio, W. E., Hazari, M. S., and Farraj, A. K. (2016). Acrolein inhalation alters myocardial synchrony and performance at and below exposure concentrations that cause ventilatory responses. Cardiovasc. Toxicol. 17, 97-108.
59. Tirumalai, R., Rajesh Kumar, T., Mai, K. H., and Biswal, S. (2002). Acrolein causes transcriptional induction of phase II genes by activation of Nrf2 in human lung type II epithelial (A549) cells. Toxicol. Lett. 132, 27-36.
60. Tracy, R. P., Lemaitre, R. N., Psaty, B. M., Ives, D. G., Evans, R. W., Cushman, M., Meilahn, E. N., and Kuller, L. H. (1997). Relationship of C-reactive protein to risk of cardiovascular disease in the elderly. Results from the Cardiovascular Health Study and the Rural Health Promotion Project. Arterioscler. Thromb. Vasc. Biol. 17, 1121-1127.
61. Trosini-Desert, V., Germaud, P., and Dautzenberg, B. (2004). Tobacco smoke and risk of bacterial infection. Rev. Mal. Respir. 21, 539-547.
62. Vladykovskaya, E., Sithu, S. D., Haberzettl, P., Wickramasinghe, N. S., Merchant, M. L., Hill, B. G., McCracken, J., Agarwal, A., Dougherty, S., Gordon, S. A., et al. (2012). Lipid peroxidation product 4-hydroxy-trans-2-nonenal causes endothelial activation by inducing endoplasmic reticulum stress. J. Biol. Chem. 287, 11398-11409.
63. Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., Bohm, M., and Nickenig, G. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. N. Engl. J. Med. 353, 999-1007.
64. Werner, N., Wassmann, S., Ahlers, P., Kosiol, S., and Nickenig, G. (2006). Circulating CD31+/annexin V+ apoptotic microparticles correlate with coronary endothelial function in patients with coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 26, 112-116.
65. Wetzelberger, K., Baba, S. P., Thirunavukkarasu, M., Ho, Y. S., Maulik, N., Barski, O. A., Conklin, D. J., and Bhatnagar, A. (2010). Postischemic deactivation of cardiac aldose reductase: Role of glutathione S-transferase P and glutaredoxin in regeneration of reduced thiols from sulfenic acids. J. Biol. Chem. 285, 26135-26148.
66. Wheat, L. A., Haberzettl, P., Hellmann, J., Baba, S. P., Bertke, M., Lee, J., McCracken, J., O'Toole, T. E., Bhatnagar, A., and Conklin, D. J. (2011). Acrolein inhalation prevents vascular endothelial growth factor-induced mobilization of flk-1+/sca-1+ cells in mice. Arterioscler. Thromb. Vasc. Biol. 31, 1598-1606.
67. Wood, R., Eichel, L., Messing, E. M., and Schwarz, E. (2001). Automated noninvasive measurement of cyclophosphamide-induced changes in murine micturition frequency and volume and demonstration of pharmacologic sensitivity. Urology 57, 115-116.
68. Woodruff, T. J., Wells, E. M., Holt, E. W., Burgin, D. E., and Axelrad, D. A. (2007). Estimating risk from ambient concentrations of acrolein across the United States. Environ. Health Perspect. 115, 410-415.
69. Zhang, H., and Forman, H. J. (2008). Acrolein induces heme oxygenase-1 through PKC-delta and PI3K in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 38, 483-490.