SP-A and SP-D surfactant proteins and conventional risk factors for chronic non-infectious human diseases
https://doi.org/10.18699/SSMJ20230303
Abstract
Surfactant proteins SP-A and SP-D, which belong to the family of collagen-containing type C lectins, are used as diagnostic and prognostic markers for many acute and chronic respiratory diseases. The aim of the study is to assess the impact of conventional risk factors for chronic non-infectious diseases on SP-A and SP-D protein levels by means of systemic and structural analysis on the basis of relevant publications from international databases and official WHO reports. This analytical review concludes that widespread expression of SP-A and SP-D is documented in numerous studies, and, although the lungs remain the main site of synthesis of surfactant proteins, one can expect its significant impact on the immune and inflammatory response in many organs and tissues. The authors note that there are several known extrapulmonary effects of these proteins. However, many mechanisms of additional cellular effects of SP-A and SP-D outside the bronchopulmonary system still remain unstudied, which indicates the prospects for further research in this area.
About the Authors
K. Yu. Nikolaev
Research Institute of Internal and Prevention Medicine – Branch of the Federal Research Center Institute of Cytology and Genetics of SB RAS; Novosibirsk State University; Surgut State University
Russian Federation
Russian Federation
Konstantin Yu. Nikolaev, doctor of medical sciences, professor
630089, Novosibirsk, Borisa Bogatkova str., 175/1
630090, Novosibirsk, Pirogova str., 2
628412, Surgut, Lenina ave., 1
O. S. Kharlamova
Research Institute of Internal and Prevention Medicine – Branch of the Federal Research Center Institute of Cytology and Genetics of SB RAS
Russian Federation
Russian Federation
Olga S. Kharlamova, candidate of medical sciences
630089, Novosibirsk, Borisa Bogatkova str., 175/1
I. A. Kosarev
Research Institute of Internal and Prevention Medicine – Branch of the Federal Research Center Institute of Cytology and Genetics of SB RAS
Russian Federation
Russian Federation
Ilya A. Kosarev
630089, Novosibirsk, Borisa Bogatkova str., 175/1
N. F. Dadashova
Surgut State University
Russian Federation
Russian Federation
Nazly F. Dadashova
628412, Surgut, Lenina ave., 1
Ya. K. Lapitskaya
Novosibirsk State University
Russian Federation
Russian Federation
Yana K. Lapitskaya
630090, Novosibirsk, Pirogova str., 2
References
1. Vieira F., Kung J.W., Bhatti F. Structure, genetics and function of the pulmonary associated surfactant proteins A and D: The extra-pulmonary role of these C type lectins. Ann. Anat. 2017;211:184–201. doi: 10.1016/j.aanat.2017.03.002
2. Watson A., Madsen J., Clark H.W. SP-A and SPD: dual functioning immune molecules with antiviral and immunomodulatory properties. Front. Immunol. 2021;11:622598. doi: 10.3389/fimmu.2020.622598
3. Liu Z., Shi Q., Liu J., Abdel-Razek O., Xu Y., Cooney R.N., Wanga G. Innate immune molecule surfactant protein d attenuates sepsis-induced acute pancreatic injury through modulating apoptosis and NF- κB-mediated inflammation. Sci. Rep. 2015;5:17798. doi: 10.1038/srep17798
4. Saka R., Wakimoto T., Nishiumi F., Sasaki T., Nose S., Fukuzawa M., Oue T., Yanagihara I., Okuyama H. Surfactant protein-D attenuates the lipopolysaccharide-induced inflammation in human intestinal cells overexpressing toll-like receptor 4. Pediatr. Surg. Int. 2016;32(1):59–63. doi: 10.1007/s00383-015-3812-y
5. Wang K., Ju Q., Cao J., Tang W., Zhang J. Impact of serum SP-A and SP-D levels on comparison and prognosis of idiopathic pulmonary fibrosis: A systematic review and meta-analysis. Medicine (Baltimore). 2017;96(23):e7083. doi: 10.1097/MD.0000000000007083
6. Sorensen G. Surfactant protein D in respiratory and non-respiratory diseases. Front. Med. (Lausanne). 2018;5:18. doi: 10.3389/fmed.2018.00018
7. Kharlamova 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. Byulleten’ sibirskoy meditsiny = Bulletin of Siberian Medicine. 2020;19(2):104–111. [In Russian]. doi: 10.20538/1682-0363-2020-2-104-111
8. Nayak A., Dodagatta-Marri E., Tsolaki A.G., Kishore U. An insight into the diverse roles of surfactant proteins, SP-A and SP-D in innate and adaptive immunity. Front. Immunol. 2012;3:131. doi: 10.3389/fimmu.2012.00131
9. Colmorten K., Nexoe A., Sorensen G. The dual role of surfactant protein-D in vascular inflammation and development of cardiovascular disease. Front. Immunol. 2019;10:2264. doi: 10.3389/fimmu.2019.02264
10. World Health Organization (2019). The top 10 causes of death. Available at: https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-ofdeath. [In Russian].
11. Ahmad F.B., Anderson R.N. The leading causes of death in the US for 2020. JAMA. 2021;325(18):1829–1830. doi: 10.1001/jama.2021.5469
12. Yasmin H., Kishore U. Biological activities of SP-A and SP-D against extracellular and intracellular pathogens. In: The Collectin Protein Family and Its Multiple Biological Activities. Springer, Cham, 2021. P. 103–133. doi: 10.1007/978-3-030-67048-1_5
13. Jakel A., Qaseem A.S., Kishore U., Sim R.B. Ligands and receptors of lung surfactant proteins SP-A and SP-D. Front. Biosci. (Landmark ed.). 2013;18:1129–1140. doi: 10.2741/4168
14. Heath C.J., del Mar Cendra M., Watson A., Auger J.-P., Pandey A., Tighe P., Christodoulides M. Cotranscriptomes of initial interactions in vitro between streptococcus pneumoniae and human pleural mesothelial cells. PloS One. 2015;10(11):e0142773. doi: 10.1371/journal.pone.0142773
15. Carreto-Binaghi L.E., Aliouat el M., Taylor M.L. Surfactant proteins, SP-A and SP-D, in respiratory fungal infections: their role in the inflammatory response. Respir. Res. 2016;17(1):66. doi: 10.1186/s12931-016-0385-9
16. Ordonez S.R., Eijk M., Escobar Salazar N., de Cock H., Veldhuizen E.J.A., Haagsman H.P. Antifungal activities of surfactant protein D in an environment closely mimicking the lung lining. Mol. Immunol. 2019;105:260–269. doi: 10.1016/j.molimm.2018.12.003
17. Kishore U., Bulla R., Madan T. Editorial: Odyssey of surfactant proteins SP-A and SP-D: innate immune surveillance molecules. Front. Immunol. 2020;11:394. doi: 10.3389/fimmu.2020.00394
18. Ujma S., Carse S., Chetty A., Horsnell W., Clark H., Madsen J., Mackay R.-M., Watson A., Griffiths M., Katz A.A., Schäfer G. Surfactant protein A impairs genital HPV16 pseudovirus infection by innate immune cell activation in a murine model. Pathogens. 2019;8(4):288. doi: 10.3390/pathogens8040288
19. Georgescu S.R., Mitran C.I., Mitran M.I., Caruntu C., Sarbu M.I., Matei C., Nicolae I., Tocut S.M., Popa M.I., Tampa M. New insights in the pathogenesis of HPV Infection and the associated carcinogenic processes: the role of chronic inflammation and oxidative stress. J. Immunol. Res. 2018;2018:5315816. doi: 10.1155/2018/5315816
20. Favier A.L., Reynard O., Gout E., van Eijk M., Haagsman H.P., Crouch E., Volchkov V., Peyrefitte C., Thielens N.M. Involvement of surfactant protein D in Ebola virus infection enhancement via glycoprotein interaction. Viruses. 2018;11(1):15. doi: 10.3390/v11010015
21. Magnan A., Botturi K., Pipet A., Cavaillès A., Reboulleau D., Langelot M., Lacoeuille Y., Berthoux E., Neveu B. Asthma exacerbations: a paradigm of synergy between allergens, pollutants and viruses. In: Allergens and Respiratory Pollutants. Cambridge: Woodhead Publishing, 2011. P. 89–116. doi: 10.1533/9781908818065.89
22. Kendall M., Ding P., Mackay R.M., Deb R., Mc-Kenzie Z., Kendall K., Madsen J., Clark H. Surfactant protein D (SP-D) alters cellular uptake of particles and nanoparticles. Nanotoxicology. 2013;7(5):963–973. doi: 10.3109/17435390.2012.689880
23. Sapkota M., Kharbanda K.K., Wyatt T.A. Malondialdehyde-acetaldehyde-adducted surfactant protein alters macrophage functions through scavenger receptor A. Alcohol. Clin. Exp. Res. 2016;40(12):2563–2572. doi: 10.1111/acer.13248
24. Mukherjee S., Giamberardino C., Thomas J., Evans K., Goto H., Ledford J.G., Hsia B., Pastva A.M., Wright J.R. Surfactant protein A integrates activation signal strength to differentially modulate T cell proliferation. J. Immunol. 2012;188(3):957–967. doi: 10.4049/jimmunol.1100461
25. Watson A., Spalluto C.M., McCrae C., Cellura D., Burke H., Cunoosamy D., Freeman A., Hicks A., Hühn M., Ostridge K., ... Wilkinson T. Dynamics of IFN-β Responses during respiratory viral infection. Insights for therapeutic strategies. Am. J. Respir. Crit. Care Med. 2020;201(1):83–94. doi: 10.1164/rccm.201901-0214OC
26. Djiadeu P., Kotra L.P., Sweezey N., Palaniyar N. Surfactant protein D delays Fas- and TRAIL-mediated extrinsic pathway of apoptosis in T cells. Apoptosis. 2017;22(5):730–740. doi: 10.1007/s10495-017-1348-4
27. Ge M.Q., Kokalari B., Flayer C.H., Killingbeck S.S., Redai I.G., MacFarlane 4th A.W., Hwang J.W., Kolupoti A., Kemeny D.M., Campbell K.S., Haczku A. Correction: cutting edge: role of NK cells and surfactant protein D in dendritic cell lymph node homing: effects of ozone exposure. J. Immunol. 2016;196(7):3212. doi: 10.4049/jimmunol.1600095
28. Barrow A.D., Palarasah Y., Bugatti M., Holehouse A.S., Byers D.E., Holtzman M.J., Vermi W., Skjødt K., Crouch E., Colonna M. OSCAR is a receptor for surfactant protein D that activates TNF-α release from human CCR2+ inflammatory monocytes. J. Immunol. 2015;194(7):3317–3326. doi: 10.4049/jimmunol.1402289
29. Olde Nordkamp M.J., van Eijk M., Urbanus R.T., Bont L., Haagsman H.P., Meyaard L. Leu-kocyte-associated Ig-like receptor-1 is a novel inhibitory receptor for surfactant protein D. J. Leukoc. Biol. 2014;96(1):105–111. doi: 10.1189/jlb.3AB0213-092RR
30. Cao X. COVID-19: immunopathology and its implications for therapy. Nat. Rev. Immunol. 2020;20(5):269–270. doi: 10.1038/s41577-020-0308-3
31. Chailley-Heu B., Rubio S., Rougier J.P., Ducroc R., Barlier-Mur A.M., Ronco P., Bourbon J.R. Expression of hydrophilic surfactant proteins by mesentery cells in rat and man. Biochem. J. 1997;328(Pt 1):251–256. doi: 10.1042/bj3280251
32. Luo J.M., Liu Z.Q., Eugene C.Y. Overexpression of pulmonary surfactant protein A like molecules in inflammatory bowel disease tissues. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2008;33(11):979–986.
33. Schob S., Dieckow J., Fehrenbach M., Peukert N., Weiss A., Kluth D., Thome U., Quäschling U., Lacher M., Preuß M. Occurrence and colocalization of surfactant proteins A, B, C and D in the developing and adult rat brain. Ann. Anat. 2017;210:121–127. doi: 10.1016/j.aanat.2016.10.006
34. Madsen J., Kliem A., Tornoe I., Skjodt K., Koch C., Holmskov U. Localization of lung surfactant protein D on mucosal surfaces in human tissues. J. Immunol. 2000;164(11):5866–5870. doi: 10.4049/jimmunol.164.11.5866
35. Kankavi O., Baykara M., Eren Karanis M.I., Bassorgun C.I., Ergin H., Ciftcioglu M.A. Evidence of surfactant protein A and D expression decrement and their localizations in human prostate adenocarcinomas. Ren. Fail. 2014;36(2):258–265. doi: 10.3109/0886022X.2013.846831
36. Snegovskikh V.V., Bhandari V., Wright J.R., Tadesse S., Morgan T., Macneill C., Foyouzi N., Park J.S., Wang Y., Norwitz E.R. Surfactant protein-A (SP-A) selectively inhibits prostaglandin F2alpha (PGF2alpha) production in term decidua: implications for the onset of labor. J. Clin. Endocrinol. Metab. 2011;96(4):624–632. doi: 10.1210/jc.2010-1496
37. Wang T., Li K., Xiao S., Xia Y. A plausible role for collectins in skin immune homeostasis. Front. Immunol. 2021;12:594858. doi: 10.3389/fimmu.2021.594858
38. Sorensen G.L., Hjelmborg J.B., Kyvik K.O., Fenger M., Hoj A., Bendixen C., Sørensen T.I.A., Holmskov U. Genetic and environmental influences of surfactant protein D serum levels. Am. J. Physiol. Lung. Cell Mol. Physiol. 2006;290(5):1010–1017. doi: 10.1152/ajplung.00487.2005
39. Ilumets H., Mazur W., Toljamo T., Louhelainen N., Nieminen P., Kobayashi H., Ishikawa N., Kinnula V.L. 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
40. Beaglehole R., Bonita R., Horton R., Adams C., Alleyne G., Asaria P., Baugh V., Bekedam H., Billo N., Casswell S., … Watt J. Priority actions for the noncommunicable disease crisis. Lancet. 2011;377(9775): 1438–1447. doi: 10.1016/S0140-6736(11)60393-0
41. Viklund E., Bake B., Hussain-Alkhateeb L., Koca Akdeva H., Larsson P., Olin A.C. Current smoking alters phospholipid- and surfactant protein A levels in small airway lining fluid: An explorative study on exhaled breath. PLoS One. 2021;16(6):e0253825. doi: 10.1371/journal.pone.0253825
42. Nida, Lone K.P. 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
43. Kobayashi H., Kanoh S., Motoyoshi K. Serum surfactant protein-A, but not surfactant protein-D or KL-6, can predict preclinical lung damage induced by smoking. Biomarkers. 2008;13(4):385–392. doi: 10.1080/13547500801903651
44. Wang Z., Xu M., Wang Y., Wang T., Wu N., Zheng W., Duan H. Air particulate matter pollution and circulating surfactant protein: A systemic review and meta-analysis. Chemosphere. 2021;272:129564. doi: 10.1016/j.chemosphere.2021.129564
45. Wulf-Johansson H., Thinggaard M., Tan Q., Johansson S.L., Schlosser A., Christensen K., Holmskov U., Sorensen G.L. Circulating surfactant protein D is associated to mortality in elderly women: a twin study. Immunobiology. 2013;218(5):712–717. doi: 10.1016/j.imbio.2012.08.272
46. Nybo M., Andersen K., Sorensen G.L., Lolk A., Kragh-Sorensen P., Holmskov U. Serum surfactant protein D is correlated to development of dementia and augmented mortality. Clin. Immunol. 2007;123(3):333–337. doi: 10.1016/j.clim.2007.03.001
47. Williams M.C., Murchison J.T., Edwards L.D., Agusti A., Bakke P., Calverley P.M., Celli B., Coxson H.O., Crim C., Lomas D.A., … MacNee W. Coronary artery calcification is increased in patients with COPD and associated with increased morbidity and mortality. Thorax. 2014;69(8):718–723. doi: 10.1136/thoraxjnl-2012-203151
48. Fisher K.A., Stefan M.S., Darling C., Lessard D., Goldberg R.J. Impact of COPD on the mortality and treatment of patients hospitalized with acute decompensated heart failure: the Worcester Heart Failure Study. Chest. 2015;147(3):637–645. doi: 10.1378/chest.14-0607
49. Gargiulo P., Banfi C., Ghilardi S., Magrì D., Giovannardi M., Bonomi A., Salvioni E., Battaia E., Filardi P.P., Tremoli E., Agostoni P. Surfactant-derived proteins as markers of alveolar membrane damage in heart failure. PLoS One. 2014;9(12):e115030. doi: 10.1371/journal.pone.0115030
50. Beketov V.D., Lebedeva M.V., Mukhin N.A., Serova A.G., Ponomarev A.B., Popova E.N., Yanakaeva A.Sh., Solomka V.A., Kondrashov A.V., Konovalov D.V. Clinical significance of the determination of surfactant proteins A and D in assessing the activity of lung sarcoidosis. Terapevticheskiy arkhiv = Therapeutic Archive. 2018;90(3):42–46. [In Russian].
51. Kati C., Alacam H., Duran L., Guzel A., Akdemir H.U., Sisman B., Sahin C., Yavuz Y., Altintas N., Murat N., Okuyucu A. The effectiveness of the serum surfactant protein D (Sp-D) level to indicate lung injury in pulmonary embolism. Clin. Lab. 2014;60(9):1457–1464. doi: 10.7754/clin.lab.2013.131009
52. Sorensen G.L., Bladbjerg E.M., Steffensen R., Tan Q., Madsen J., Drivsholm T., Holmskov U. Association between the surfactant protein D (SFTPD) gene and subclinical carotid artery atherosclerosis. Atherosclerosis. 2016;246:7–12. doi: 10.1016/j.atherosclerosis. 2015.12.037
53. Hill J., Heslop C., Man S.F., Frohlich J., Connett J.E., Anthonisen N.R., Wise R.A., Tashkin D.P., Sin D.D. Circulating surfactant protein-D and the risk of cardiovascular morbidity and mortality. Eur. Heart. J. 2011;32(15):1918–1925. doi: 10.1093/eurheartj/ehr124
54. Maev I.V., Lyamina S.V., Kalish S.V., Yurenev G.L., Malyshev I.Yu. Total content and oligomeric transformations of surfactant protein d in bronchoalveolar lavage fluid in bronchial asthma and gastroesophageal reflux disease: role in impaired immune response. Klinicheskaya meditsina = Clinical Medicine. 2013;91(4):33–38. [In Russian].
55. Wannamethee S.G., Shaper A.G., Rumley A., Sattar N., Whincup P.H., Thomas M.C., Lowe G.D. Lung function and risk of type 2 diabetes and fatal and nonfatal major coronary heart disease events: possible associations with inflammation. Diabetes Care. 2010;33(9):1990–1996. doi: 10.2337/dc10-0324
56. Kolahian S., Leiss V., Nürnberg B. Diabetic lung disease: fact or fiction? Rev. Endocr. Metab. Disord. 2019;20(3):303–319. doi: 10.1007/s11154-019-09516-w
57. Yeh F., Dixon A.E., Marion S., Schaefer C., Zhang Y., Best L.G., Calhoun D., Rhoades E.R., Lee E.T. Obesity in adults is associated with reduced lung function in metabolic syndrome and diabetes: the Strong Heart Study. Diabetes Care. 2011;34(10):2306–2313. doi: 10.2337/dc11-0682
58. Fernández-Real J.M., Valdés S., Manco M., Chico B., Botas P., Campo A., Casamitjana R., Delgado E., Salvador J., Fruhbeck G., Mingrone G., Ricart W. Surfactant protein D, a marker of lung innate immunity, is positively associated with insulin sensitivity. Diabetes Care. 2010;33(4):847–853. doi: 10.2337/dc09-0542
59. Keating E., Rahman L., Francis J., Petersen A., Possmayer F., Veldhuizen R., Petersen N.O. Effect of cholesterol on the biophysical and physiological properties of a clinical pulmonary surfactant. Biophys. J. 2007;93(4):1391–401. doi: 10.1529/biophysj.106.099762
60. Rezaei S., Shamsi M.M., Mahdavi M., Jamali A., Prestes J., Tibana R.A., Navalta J.W., Voltarelli F.A. Endurance exercise training decreased serum levels of surfactant protein D and improved aerobic fitness of obese women with type-2 diabetes. Diabetol. Metab. Syndr. 2017;9:74. doi: 10.1186/s13098-017-0273-6
61. Hoyt L.R., Ather J.L., Randall M.J., DePuccio D.P., Landry C.C., Wewers M.D., Gavrilin M.A., Poynter M.E. Ethanol and other short-chain alcohols inhibit NLRP3 inflammasome activation through protein tyrosine phosphatase stimulation. J. Immunol. 2016;197(4):1322–1334. doi: 10.4049/jimmunol.1600406
62. Ng H.P., Jennings S., Nelson S., Wang G. Shortchain alcohols upregulate GILZ gene expression and attenuate LPS-induced septic immune response. Front. Immunol. 2020;11:53. doi: 10.3389/fimmu.2020.00053
Review
For citations:
Nikolaev K.Yu., Kharlamova O.S., Kosarev I.A., Dadashova N.F., Lapitskaya Ya.K. SP-A and SP-D surfactant proteins and conventional risk factors for chronic non-infectious human diseases. Сибирский научный медицинский журнал. 2023;43(3):28-38. (In Russ.) https://doi.org/10.18699/SSMJ20230303
Views:
1654
Email this article 