Disruption of the structural and functional features of surfactant protein A by acrolein in cigarette smoke

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Takamiya, Rina ^a   Uchida, Koji ^b   Shibata, Takahiro ^b   Maeno, Toshitaka ^c   Kato, Masaki ^d   Yamaguchi, Yoshiki ^d   Ariki, Shigeru ^a   Hasegawa, Yoshihiro ^a   Saito, Atsushi ^a   Miwa, Soichi ^e   Takahashi, Hiroki ^a   Akaike, Takaaki ^f   Kuroki, Yoshio ^a   Takahashi, Motoko ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d RIKEN   (Japan)

^e HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACROLEIN; ALDEHYDE; SURFACTANT PROTEIN A; THIOL DERIVATIVE;

ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL LINE; CIGARETTE SMOKING; CRICETULUS; FEMALE; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOUSE; PHAGOCYTOSIS; PROTEIN CONFORMATION; RAW 264.7 CELL LINE; TOBACCO;

ACROLEIN; ALDEHYDES; ANIMALS; CHO CELLS; CIGARETTE SMOKING; CRICETULUS; FEMALE; MACROPHAGES; MICE; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PHAGOCYTOSIS; PROTEIN CONFORMATION; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; RAW 264.7 CELLS; SULFHYDRYL COMPOUNDS; TOBACCO;

EID: 85027488478     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-08588-5     Document Type: Article

References (56)

1. Barnes, P. J. Chronic obstructive pulmonary disease. N Engl J Med 343, 269-280, doi:10.1056/NEJM200007273430407 (2000).
2. Talhout, R. et al. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health 8, 613-628, doi:10.3390/ijerph8020613 (2011).
3. Uchida, K. et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci USA 95, 4882-4887 (1998).
4. Hristova, M. et al. The tobacco smoke component, acrolein, suppresses innate macrophage responses by direct alkylation of c-Jun N-terminal kinase. Am J Respir Cell Mol Biol 46, 23-33, doi:10.1165/rcmb.2011-0134OC (2012).
5. Furuhata, A. et al. N(epsilon)-(3-methylpyridinium)lysine, a major antigenic adduct generated in acrolein-modified protein. J Biol Chem 278, 48658-48665, doi:10.1074/jbc.M309401200 (2003).
6. Uchida, K. et al. Acrolein is a product of lipid peroxidation reaction. Formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 273, 16058-16066 (1998).
7. Kirkham, P. A., Spooner, G., Rahman, I. & Rossi, A. G. Macrophage phagocytosis of apoptotic neutrophils is compromised by matrix proteins modified by cigarette smoke and lipid peroxidation products. Biochem Biophys Res Commun 318, 32-37, doi:10.1016/j.bbrc.2004.04.003 (2004).
8. Tran, T. N. et al. Acrolein modification impairs key functional features of rat apolipoprotein E: identification of modified sites by mass spectrometry. Biochemistry 53, 361-375, doi:10.1021/bi401404u (2014).
9. Kenche, H. et al. Adverse Outcomes Associated with Cigarette Smoke Radicals Related to Damage to Protein-disulfide Isomerase. J Biol Chem 291, 4763-4778, doi:10.1074/jbc.M115.712331 (2016).
10. Crouch, E. & Wright, J. R. Surfactant proteins a and d and pulmonary host defense. Annu Rev Physiol 63, 521-554, doi:10.1146/annurev.physiol.63.1.521 (2001).
11. McCormack, F. X. & Whitsett, J. A. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J Clin Invest 109, 707-712, doi:10.1172/JCI15293 (2002).
12. Wright, J. R. Immunoregulatory functions of surfactant proteins. Nat Rev Immunol 5, 58-68, doi:10.1038/nri1528 (2005).
13. Kuroki, Y. & Akino, T. Pulmonary surfactant protein A (SP-A) specifically binds dipalmitoylphosphatidylcholine. J Biol Chem 266, 3068-3073 (1991).
14. Yu, S. H., McCormack, F. X., Voelker, D. R. & Possmayer, F. Interactions of pulmonary surfactant protein SP-A with monolayers of dipalmitoylphosphatidylcholine and cholesterol: roles of SP-A domains. J Lipid Res 40, 920-929 (1999).
15. Van Iwaarden, J. F. et al. Binding of surfactant protein A to the lipid A moiety of bacterial lipopolysaccharides. Biochem J 303(Pt 2), 407-411 (1994).
16. Woodworth, B. A., Wood, R., Baatz, J. E. & Schlosser, R. J. Sinonasal surfactant protein A1, A2, and D gene expression in cystic fibrosis: a preliminary report. Otolaryngol Head Neck Surg 137, 34-38, doi:10.1016/j.otohns.2007.01.025 (2007).
17. Shang, F. et al. Crystallographic complexes of surfactant protein A and carbohydrates reveal ligand-induced conformational change. J Biol Chem 286, 757-765, doi:10.1074/jbc.M110.175265 (2011).
18. Goh, B. C. et al. Elucidation of Lipid Binding Sites on Lung Surfactant Protein A Using X-ray Crystallography, Mutagenesis, and Molecular Dynamics Simulations. Biochemistry 55, 3692-3701, doi:10.1021/acs.biochem.6b00048 (2016).
19. Honda, Y., Takahashi, H., Kuroki, Y., Akino, T. & Abe, S. Decreased contents of surfactant proteins A and D in BAL fluids of healthy smokers. Chest 109, 1006-1009 (1996).
20. Subramaniam, S., Whitsett, J. A., Hull, W. & Gairola, C. G. Alteration of pulmonary surfactant proteins in rats chronically exposed to cigarette smoke. Toxicol Appl Pharmacol 140, 274-280, doi:10.1006/taap.1996.0222 (1996).
21. Kida, K., Oda, H., Yamano, Y. & Kagawa, J. Effects of cigarette smoking on the serum concentration of lung surfactant protein A (SP-A). Eur Respir J 10, 2124-2126 (1997).
22. Nomori, H. et al. Serum surfactant protein A levels in healthy individuals are increased in smokers. Lung 176, 355-361 (1998).
23. Mazur, W. et al. Elevation of surfactant protein A in plasma and sputum in cigarette smokers. Eur Respir J 38, 277-284, doi:10.1183/09031936.00110510 (2011).
24. Betsuyaku, T., Kuroki, Y., Nagai, K., Nasuhara, Y. & Nishimura, M. Effects of ageing and smoking on SP-A and SP-D levels in bronchoalveolar lavage fluid. Eur Respir J 24, 964-970, doi:10.1183/09031936.04.00064004 (2004).
25. Larstad, M. et al. Surfactant Protein A in Exhaled Endogenous Particles Is Decreased in Chronic Obstructive Pulmonary Disease (COPD) Patients: A Pilot Study. PLoS One 10, e0144463, doi:10.1371/journal.pone.0144463 (2015).
26. Ohlmeier, S. et al. Proteomics of human lung tissue identifies surfactant protein A as a marker of chronic obstructive pulmonary disease. J Proteome Res 7, 5125-5132, doi:10.1021/pr800423x (2008).
27. Shibata, Y. et al. Altered expression of antimicrobial molecules in cigarette smoke-exposed emphysematous mice lungs. Respirology 13, 1061-1065, doi:10.1111/j.1440-1843.2008.01362.x (2008).
28. Stampfli, M. R. & Anderson, G. P. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9, 377-384, doi:10.1038/nri2530 (2009).
29. Brusselle, G. G., Joos, G. F. & Bracke, K. R. New insights into the immunology of chronic obstructive pulmonary disease. Lancet 378, 1015-1026, doi:10.1016/S0140-6736(11)60988-4 (2011).
30. Kuzmenko, A. I., Wu, H., Bridges, J. P. & McCormack, F. X. Surfactant lipid peroxidation damages surfactant protein A and inhibits interactions with phospholipid vesicles. J Lipid Res 45, 1061-1068, doi:10.1194/jlr.M300360-JLR200 (2004).
31. Kitaguchi, Y. et al. Acrolein induces endoplasmic reticulum stress and causes airspace enlargement. PLoS One 7, e38038, doi:10.1371/journal.pone.0038038 (2012).
32. Furuhata, A., Nakamura, M., Osawa, T. & Uchida, K. Thiolation of protein-bound carcinogenic aldehyde. An electrophilic acroleinlysine adduct that covalently binds to thiols. J Biol Chem 277, 27919-27926, doi:10.1074/jbc.M202794200 (2002).
33. Burcham, P. C., Fontaine, F. R., Petersen, D. R. & Pyke, S. M. Reactivity with Tris(hydroxymethyl)aminomethane confounds immunodetection of acrolein-adducted proteins. Chem Res Toxicol 16, 1196-1201, doi:10.1021/tx0341106 (2003).
34. Adachi, T. et al. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10, 1200-1207, doi:10.1038/nm1119 (2004).
35. Sreerama, N. & Woody, R. W. Computation and analysis of protein circular dichroism spectra. Methods Enzymol 383, 318-351, doi:10.1016/S0076-6879(04)83013-1 (2004).
36. Greenfield, N. J. Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1, 2876-2890, doi:10.1038/nprot.2006.202 (2006).
37. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201, doi:10.1093/bioinformatics/bti770 (2006).
38. Wu, H. et al. Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability. J Clin Invest 111, 1589-1602, doi:10.1172/JCI16889 (2003).
39. van Iwaarden, F., Welmers, B., Verhoef, J., Haagsman, H. P. & van Golde, L. M. Pulmonary surfactant protein A enhances the hostdefense mechanism of rat alveolar macrophages. Am J Respir Cell Mol Biol 2, 91-98, doi:10.1165/ajrcmb/2.1.91 (1990).
40. Yamada, C. et al. Surfactant protein A directly interacts with TLR4 and MD-2 and regulates inflammatory cellular response. Importance of supratrimeric oligomerization. J Biol Chem 281, 21771-21780, doi:10.1074/jbc.M513041200 (2006).
41. Awasthi, S., Madhusoodhanan, R. & Wolf, R. Surfactant protein-A and toll-like receptor-4 modulate immune functions of preterm baboon lung dendritic cell precursor cells. Cell Immunol 268, 87-96, doi:10.1016/j.cellimm.2011.02.009 (2011).
42. Oliveira, E. C., Marik, P. E. & Colice, G. Influenza pneumonia: a descriptive study. Chest 119, 1717-1723 (2001).
43. Sever-Chroneos, Z. et al. Surfactant protein A (SP-A)-mediated clearance of Staphylococcus aureus involves binding of SP-A to the staphylococcal adhesin eap and the macrophage receptors SP-A receptor 210 and scavenger receptor class A. J Biol Chem 286, 4854-4870, doi:10.1074/jbc.M110.125567 (2011).
44. Maeno, T. et al. CD8+T Cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol 178, 8090-8096 (2007).
45. Logan, J. et al. Brief exposure to cigarette smoke impairs airway epithelial cell innate anti-viral defence. Toxicol In Vitro 28, 1430-1435, doi:10.1016/j.tiv.2014.07.012 (2014).
46. O'Leary, S. M. et al. Cigarette smoking impairs human pulmonary immunity to Mycobacterium tuberculosis. Am J Respir Crit Care Med 190, 1430-1436, doi:10.1164/rccm.201407-1385OC (2014).
47. Moretto, N., Volpi, G., Pastore, F. & Facchinetti, F. Acrolein effects in pulmonary cells: relevance to chronic obstructive pulmonary disease. Ann N Y Acad Sci 1259, 39-46, doi:10.1111/j.1749-6632.2012.06531.x (2012).
48. Sanchez-Barbero, F., Strassner, J., Garcia-Canero, R., Steinhilber, W. & Casals, C. Role of the degree of oligomerization in the structure and function of human surfactant protein A. J Biol Chem 280, 7659-7670, doi:10.1074/jbc.M410266200 (2005).
49. Head, J. F., Mealy, T. R., McCormack, F. X. & Seaton, B. A. Crystal structure of trimeric carbohydrate recognition and neck domains of surfactant protein A. J Biol Chem 278, 43254-43260, doi:10.1074/jbc.M305628200 (2003).
50. Jaspers, I. Cigarette smoke effects on innate immune mechanisms in the nasal mucosa. Potential effects on the microbiome. Ann Am Thorac Soc 11(Suppl 1), S38-42, doi:10.1513/AnnalsATS.201306-154MG (2014).
51. Qiu, Y. et al. Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 168, 968-975, doi:10.1164/rccm.200208-794OC (2003).
52. Wedzicha, J. A. & Seemungal, T. A. COPD exacerbations: defining their cause and prevention. Lancet 370, 786-796, doi:10.1016/S0140-6736(07)61382-8 (2007).
53. Hautamaki, R. D., Kobayashi, D. K., Senior, R. M. & Shapiro, S. D. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277, 2002-2004 (1997).
54. Takamiya, R. et al. Resolvin E1 maintains macrophage function under cigarette smoke-induced oxidative stress. FEBS Open Bio 2, 328-333, doi:10.1016/j.fob.2012.10.001 (2012).
55. Shibata, T. et al. Transthiocarbamoylation of proteins by thiolated isothiocyanates. J Biol Chem 286, 42150-42161, doi:10.1074/jbc.M111.308049 (2011).
56. Ariki, S. et al. Pulmonary collectins play distinct roles in host defense against Mycobacterium avium. J Immunol 187, 2586-2594, doi:10.4049/jimmunol.1100024 (2011).