Effects of smoking on the level of sp-a and sp-d surfactant proteins in the blood of patients without bronchopulmonary diseases
https://doi.org/10.20538/1682-0363-2020-2-104-111
Abstract
Every year, about six million people die from tobacco use. Respiratory epithelium is the first line of defense against exogenous invasion, in particular, harmful inhaled particles, pathogens and allergens. However, the epithelium of the respiratory tract is also a regulator of immunological and inflammatory reactions through secretion of inflammation and immune cell recruitment mediators. An important component of the pulmonary immune system is the surfactant, and, in particular, its proteins SP-A and SP-D, synthesized mainly by type II pneumocytes.
Aim. To assess the levels of surfactant proteins SP-A and SP-D in the blood of smoking patients without bronchopulmonary diseases.
Materials and мethods. The study included 59 patients admitted to the department of internal medicine with hypertension. The general group was divided into subgroups: non-smoking patients (n = 31) and healthy smokers (n = 28). All patients underwent clinical, functional, diagnostic and laboratory tests. The content of surfactant proteins SP-A and SP-D in the blood was determined by enzyme immunoassay.
Results. The subgroups did not differ in sex, age, height, body weight, blood pressure, heart rate, respiratory rate, and the distribution of comorbidities. The subgroups differed in the platelet level; in other main parameters of complete blood count and blood biochemistry no differences were revealed. It was found that the blood levels of surfactant proteins SP-A and SP-D in the subgroup of healthy smokers were significantly higher in comparison with the subgroup of non-smoking patients. The correlation analysis revealed a direct relationship between surfactant proteins SP-A and SP-D and smoking (R = 0.360, p = 0.006, R = 0.274, p = 0.037), a negative correlation between SP-D protein and age (R = –0.315, p = 0.016), and a direct relationship between SP-A protein and diastolic blood pressure (R = 0.271, p = 0.039). In the non-smoking subgroup, a negative correlation between SP-D and age (R = –0.438, p = 0.016) and between SP-D and systolic blood pressure (R = –0.433, p = 0.017) was identified.
Conclusion. The direct relationship between higher levels of the surfactant proteins SP-A and SP-D and smoking in the group of healthy smokers is justified (inflammatory changes, structural abnormalities in the lung parenchyma under the influence of cigarette smoke). The SP-D protein is more significant in comparison with the SP-A protein in vascular wall remodeling, lung tissue matrix, oxidative lung tissue damage, and apoptosis, which explains its negative correlation with age and systolic blood pressure.
About the Authors
O. S. KharlamovаRussian Federation
175/1, Boris Bogatkov Str., Novosibirsk, 630089, Russian Federation
K. Yu. Nikolaev
Russian Federation
175/1, Boris Bogatkov Str., Novosibirsk, 630089, Russian Federation
Yu. I. Ragino
Russian Federation
175/1, Boris Bogatkov Str., Novosibirsk, 630089, Russian Federation
M. I. Voevoda
Russian Federation
175/1, Boris Bogatkov Str., Novosibirsk, 630089, Russian Federation
References
1. WHO. Global Report on Trends in Prevalence of Tobacco Smoking. Geneva, Switzerland, 2015.
2. Moré J., Voelker D., Silveira L., Edwards M., Chan E., Bowler R. Smoking reduces surfactant protein D and phospholipids in patients with and without chronic obstructive pulmonary disease. BMC Pulm. Med. 2010; 10: 53. DOI: 10.1186/1471-2466-10-53.
3. Schauer G.L., Wheaton A.G., Malarcher A.M., Croft J.B. Health-care provider screening and advice for smoking cessation among smokers with and without COPD: 2009–2010 National Adult Tobacco Survey. Chest. 2016; 149 (3): 676–684. DOI: 10.1378/chest.14-2965.
4. Gutsol A.A., Blanco P., Samokhina S.I. et al. A novel method for comparison of arterial remodeling in hypertension: quantification of arterial trees and recognition of remodeling patterns on histological sections. PLoS One. 2019; 14 (5): e0216734. DOI: 10.1371/journal.pone.0216734.
5. Campos Td. S., Richter K.P., Cupertino A.P. et al. Cigarette smoking among patients with chronic diseases. Int. J. Cardiol. 2014; 174 (3): 808–810. DOI: 10.1016/j.ijcard.2014.04.150.
6. Rizzoni D., Agabiti-Rosei E. Structural abnormalities of small resistance arteries in essential hypertension. Intern. Emerg. Med. 2012; 7 (3): 205–212. DOI: 10.1007/s11739-011-0548-0.
7. Sopori M. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2002; 2: 372–377. DOI: 10.1038/nri803.
8. Laurent S., Boutouyrie P. The structural factor of hypertension: large and small artery alterations. Circ. Res. 2015; 116 (6): 1007–1021. DOI: 10.1161/CIRCRESAHA.116.303596.
9. Stampfli M.R., Anderson G.P. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol. 2009; 9 (5): 377–384. DOI: 10.1038/nri2530.
10. Hill G.S., Heudes D., Jacquot C., Gauthier E., Bariéty J. Morphometric evidence for impairment of renal autoregulation in advanced essential hypertension. Kidney Int. 2006; 69 (5): 823–831. DOI: 10.1038/sj.ki.5000163.
11. Nuorti J.P., Butler J.C., Farley M.M., Harrison L.H., McGeer A., Kolczak M.S., Breiman R.F. Cigarette smoking and invasive pneumococcal disease. Active Bacterial Core Surveillance Team. N. Engl. J. Med. 2000; 342 (10): 681–689. DOI: 10.1056/NEJM200003093421002.
12. Schoen F.J. Robbins basic pathology. In: Kumar V., Abbas A. F.N. (edit.) Pathologic basis of disease. 7th ed. Philadelphia: Elsevier Saunders; 2012: 511–554.
13. Zhang M., Shi R., Zhang Y. et al. Nix/BNIP3L‐dependent mitophagy accounts for airway epithelial cell injury induced by cigarette smoke. J. Cell Physiol. 2019; 234 (8): 1420–1422. DOI: 10.1002/jcp.28117.
14. Vandivier R., Ogden C., Fadok V. A., Hoffmann P., Brown K., Botto M., Walport M. J., Fisher J. H., Henson P. M., Greene K. E. (2002). Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 2002: 169 (7): 3978–3986. DOI: 10.4049/jimmunol.169.7.3978.
15. Zeglinski M., Turner C., Zeng R. et al. Soluble wood smoke extract promotes barrier dysfunction in alveolar epithelial cells through a MAPK signaling pathway. Sci. Rep. 2019; 9 (1): 10027. DOI: 10.1038/s41598-019-46400-8.
16. Umstead T.M., Freeman W.M., Chinchilli V.M., Phelps D.S. Age-related changes in the expression and oxidation of bronchoalveolar lavage proteins in the rat. Am. J. Physiol. Lung Cell Mol. Physiol. 2009; 296 (1): L14–29. DOI: 10.1152/ajplung.90366.2008.
17. Dye J.A., Adler K.B. Effects of cigarette smoke on epithelial cells of the respiratory tract. Thorax. 1994; 49 (8): 825–834. DOI: 10.1136/thx.49.8.825.
18. 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. 2004; 24 (6): 964–970. DOI: 10.1183/09031936.04.00064004.
19. Pastva A.M., Wright J.R., Williams K.L. Immunomodulatory roles of surfactant proteins A and D: implications in lung disease. Proc. Am. Thorac. Soc. 2007; 4 (3): 252–257. DOI: 10.1513/pats.200701-018AW.
20. Zhao X.M., Wu Y.P., Wei R., Cai H.X., Tornoe I., Han J.J. et al. Plasma surfactant protein D levels and the relation to body mass index in a chinese population. Scand. J. Immunol. 2007; 66 (1): 71–76. DOI: 10.1111/j.1365-3083.2007.01943.x.
21. Mastora I., Remy-Jardin M., Sobaszek A., Boulenguez C., Remy J., Edme J.L. Thin-section CT finding in 250 volunteers: assessment of the relationship of CT findings with smoking history and pulmonary function test results. Radiology. 2001; 218 (3): 695–702. DOI: 10.1148/radiology.218.3.r01mr08695.
22. Moliva J.I., Rajaram M.V., Sidiki S., Sasindran S.J., Guirado E., Pan X.J. et al. Molecular composition of the alveolar lining fluid in the aging lung. Age (Dordr). 2014; 36 (3): 9633. DOI: 10.1007/s11357-014-9633-4.
23. Sorensen G.L., Hjelmborg J.B., Kyvik K.O., Fenger M., Hoj A., Bendixen C. et al. Genetic and environmental influences of surfactant protein D serum levels. Am. J. Physiol. Lung Cell Mol. Physiol. 2006; 290 (5): L1010–1017. DOI: 10.1152/ajplung.00487.2005.
24. Mazur W., Tolijamo T., Ohlmeier S., Vuopala K., Nieminen P., Kobayashi H. et al. Elevation of surfactant protein A in plasma and sputum in cigarette smokers. Eur. Respir. J. 2011; 38 (2): 277–284. DOI: 10.1183/09031936.00110510.
25. Behera D., Balamugesh T., Venkateswarlu D., Gupta A., Majumdar S. Serum surfactant protein A levels in chronic bronchitis and its relation to smoking. Indian J. Chest. Dis. Allied Sci. 2005; 47 (1): 13–17.
26. Ilumets H., Mazur W., Toljamo T., Louhelainen N., Nieminen P., Kobayashi H. et al. Ageing and smoking contribute to plasma surfactant proteins and protease imbalance with correlations to airway obstruction. BMC Pulm. Med. 2011; 11: 19. DOI: 10.1186/1471-2466-11-19.
27. Moazed F., Burnham E.L., Vandivier R.W., O’Kane C.M., Shyamsundar M., Hamid U. et al. Cigarette smokers have exaggerated alveolar barrier disruption in response to lipopolysaccharide inhalation. Thorax. 2016; 71 (12): 1130–1136. DOI: 10.1136/thoraxjnl-2015-207886.
28. Lone K.P., Nida. Plasma surfactant protein-A levels in apparently healthy smokers, stable and exacerbation COPD patients. Pak. J. Med. Sci. 2018; 34 (4): 934–939. DOI: 10.12669/pjms.344.13951.
29. Hogg J.C. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet. 2004; 364 (9435): 709–721. DOI: 10.1016/S0140-6736(04)16900-6.
30. Hastings R.H., Grady M., Sakuma T., Matthay M.A. Clearance of different-sized proteins from the alveolar space in humans and rabbits. J. Appl. Physiol. 1992; 73 (4): 1310–1316. DOI: 10.1152/jappl.1992.73.4.1310.
31. Gaunsbaek M.Q, Rasmussen K.J., Beers M.F., Atochina-Vasserman E.N., Hansen S. Lung surfactant protein D (SP-D) response and regulation during acute and chronic lung injury. Lung. 2013; 191 (3): 295–303. DOI: 10.1007/s00408-013-9452-x.
32. Hirama N., Shibata Y., Otake K., Machiya J., Wada T., Inoue S. et al. Increased surfactant protein-D and foamy macrophages in smoking-induced mouse emphysema. Respirology. 2007; 12 (2): 191–201. DOI: 10.1111/j.1440-1843.2006.01009.x
33. Winkler C., Atochina-Vasserman E.N., Holz O., Beers M.F., Erpenbeck V.J., Krug N. et al. Comprehensive characterisation of pulmonary and serum surfactant protein D in COPD. Respir. Res. 2011; 12: 29. DOI: 10.1186/1465-9921-12-29.
34. Moré J., Voelker D., Silveira L., Edwards M., Chan E., Bowler R. Smoking reduces surfactant protein D and phospholipids in patients with and without chronic obstructive pulmonary disease. BMC Pulm. Med. 2010; 10: 53. DOI: 10.1186/1471-2466-10-53.
35. Gutsol A.A., Blanco P., Samokhina S.I. et al. A novel method for comparison of arterial remodeling in hypertension: quantification of arterial trees and recognition of remodeling patterns on histological sections. PLoS One. 2019; 14 (5): e0216734. DOI: 10.1371/journal.pone.0216734.
36. Rizzoni D., Agabiti-Rosei E. Structural abnormalities of small resistance arteries in essential hypertension. Intern. Emerg. Med. 2012; 7 (3): 205–212. DOI: 10.1007/s11739-011-0548-0.
37. Laurent S., Boutouyrie P. The structural factor of hypertension: large and small artery alterations. Circ. Res. 2015; 116 (6): 1007–1021. DOI: 10.1161/CIRCRESAHA.116.303596.
38. Hill G.S., Heudes D., Jacquot C., Gauthier E., Bariéty J. Morphometric evidence for impairment of renal autoregulation in advanced essential hypertension. Kidney Int. 2006; 69 (5): 823–831. DOI: 10.1038/sj.ki.5000163.
39. Schoen F.J. Robbins basic pathology. In: Kumar V., Abbas A. F.N. (edit.) Pathologic basis of disease. 7th ed. Philadelphia: Elsevier Saunders; 2012: 511–554.
40. Vandivier R., Ogden C., Fadok V. A., Hoffmann P., Brown K., Botto M., Walport M. J., Fisher J. H., Henson P. M., Greene K. E. (2002). Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 2002: 169 (7): 3978–3986. DOI: 10.4049/jimmunol.169.7.3978.
41. Umstead T.M., Freeman W.M., Chinchilli V.M., Phelps D.S. Age-related changes in the expression and oxidation of bronchoalveolar lavage proteins in the rat. Am. J. Physiol. Lung Cell Mol. Physiol. 2009; 296 (1): L14–29. DOI: 10.1152/ajplung.90366.2008.
42. 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. 2004; 24 (6): 964–970. DOI: 10.1183/09031936.04.00064004.
43. Zhao X.M., Wu Y.P., Wei R., Cai H.X., Tornoe I., Han J.J. et al. Plasma surfactant protein D levels and the relation to body mass index in a chinese population. Scand. J. Immunol. 2007; 66 (1): 71–76. DOI: 10.1111/j.1365-3083.2007.01943.x.
44. Moliva J.I., Rajaram M.V., Sidiki S., Sasindran S.J., Guirado E., Pan X.J. et al. Molecular composition of the alveolar lining fluid in the aging lung. Age (Dordr). 2014; 36 (3): 9633. DOI: 10.1007/s11357-014-9633-4.
Review
For citations:
Kharlamovа O.S., Nikolaev K.Yu., Ragino Yu.I., Voevoda M.I. Effects of smoking on the level of sp-a and sp-d surfactant proteins in the blood of patients without bronchopulmonary diseases. Bulletin of Siberian Medicine. 2020;19(2):104-111. https://doi.org/10.20538/1682-0363-2020-2-104-111