Top

Current Allergy and Asthma Reports

Published in:

01-11-2020 | Bronchial Asthma | Basic and Applied Science (I Lewkowich, Section Editor)

Pulmonary Surfactants: a New Therapeutic Target in Asthma

Authors: Youngwoo Choi, Jaehyuk Jang, Hae-Sim Park

Published in: Current Allergy and Asthma Reports | Issue 11/2020

Abstract

Purpose of Review

Lung tissues are highly susceptible to airway inflammation as they are inevitably exposed to inhaled pathogens and allergens. In the lungs, clearance of infectious agents and regulation of inflammatory responses are important for the first-line defense, where surfactants play a role in host defense mechanisms. In this review, clinical significance of pulmonary surfactants in asthma has been highlighted.

Recent Findings

Surfactants, such as surfactant protein A (SP-A) and SP-D released from alveolar epithelium, reduce pathogen infection and control immune-cell activation. Especially, SP-D directly binds to eosinophil surface, leading to inhibition of extracellular trap formation and reduction in airway inflammation. Production of surfactants is commonly determined by both genetic (single nucleotide polymorphisms) and environmental factors influencing processes involved in the development of asthma. In addition, nintedanib (an intracellular inhibitor of tyrosine kinases) could increase SP-D levels and is used in patients with idiopathic pulmonary fibrosis. These findings may provide a possible application of SP-D in asthma.

Summary

Surfactants are key players contributing to host defense through maintaining the immune system. As clinical implications of surfactants involved in asthma have been suggested, further translational studies are needed to apply surfactants as an effective therapeutic target in patients with asthma.

Nayak A, Dodagatta-Marri E, Tsolaki AG, 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. https://doi.org/10.3389/fimmu.2012.00131.CrossRefPubMedPubMedCentral

•• Wright JR. Immunoregulatory functions of surfactant proteins. Nat Rev. Immunol. 2005;5(1):58–68. https://doi.org/10.1038/nri1528 This article summarized immunoregulatory functions of surfactant proteins in various lung diseases and conditions.CrossRefPubMed

Han S, Mallampalli RK. The role of surfactant in lung disease and host defense against pulmonary infections. Ann Am Thorac Soc. 2015;12(5):765–74. https://doi.org/10.1513/AnnalsATS.201411-507FR.CrossRefPubMedPubMedCentral

Hohlfeld JM. The role of surfactant in asthma. Respir Res. 2002;3:4. https://doi.org/10.1186/rr176.CrossRefPubMed

Nelson RK, Bush A, Stokes J, Nair P, Akuthota P. Eosinophilic asthma. J Allergy Clin Immunol Pract. 2020;8(2):465–73. https://doi.org/10.1016/j.jaip.2019.11.024.CrossRefPubMed

Jansson SA, Backman H, Andersson M, Telg G, Lindberg A, Stridsman C, et al. Severe asthma is related to high societal costs and decreased health related quality of life. Respir Med. 2020;162:105860. https://doi.org/10.1016/j.rmed.2019.105860.CrossRefPubMed

Holguin F, Cardet JC, Chung KF, Diver S, Ferreira DS, Fitzpatrick A, et al. Management of severe asthma: a European Respiratory Society/American Thoracic Society guideline. Eur Respir J. 2020;55(1). https://doi.org/10.1183/13993003.00588-2019.

Song WJ, Lee JH, Kang Y, Joung WJ, Chung KF. Future risks in patients with severe asthma. Allergy Asthma Immunol Res. 2019;11(6):763–78. https://doi.org/10.4168/aair.2019.11.6.763.CrossRefPubMedPubMedCentral

Agache I, Cojanu C, Laculiceanu A, Rogozea L. Critical points on the use of biologicals in allergic diseases and asthma. Allergy Asthma Immunol Res. 2020;12(1):24–41. https://doi.org/10.4168/aair.2020.12.1.24.CrossRefPubMed

10.

Choi Y, Sim S, Park HS. Distinct functions of eosinophils in severe asthma with type 2 phenotype: clinical implications. Korean J Intern Med. 2020. https://doi.org/10.3904/kjim.2020.022.

11.

McDowell PJ, Heaney LG. Different endotypes and phenotypes drive the heterogeneity in severe asthma. Allergy. 2020;75(2):302–10. https://doi.org/10.1111/all.13966.CrossRefPubMed

12.

Pembrey L, Barreto ML, Douwes J, Cooper P, Henderson J, Mpairwe H, et al. Understanding asthma phenotypes: the World Asthma Phenotypes (WASP) international collaboration. ERJ Open Res. 2018;4(3). https://doi.org/10.1183/23120541.00013-2018.

13.

• Holgate ST. Innate and adaptive immune responses in asthma. Nat Med. 2012;18(5):673–83. https://doi.org/10.1038/nm.2731 This article explained an importance of innate and adaptive immune responses in asthma.CrossRefPubMed

14.

Hirahara K, Shinoda K, Morimoto Y, Kiuchi M, Aoki A, Kumagai J, et al. Immune cell-epithelial/mesenchymal interaction contributing to allergic airway inflammation associated pathology. Front Immunol. 2019;10:570. https://doi.org/10.3389/fimmu.2019.00570.CrossRefPubMedPubMedCentral

15.

Siroux V, Bouzigon E. Asthma heterogeneity: the increasing genetic evidence. Lancet Respir Med. 2019;7(6):469–71. https://doi.org/10.1016/S2213-2600(19)30047-5.CrossRefPubMed

16.

Altman MC, Beigelman A, Ciaccio C, Gern JE, Heymann PW, Jackson DJ, et al. Evolving concepts in how viruses impact asthma: a work group report of the Microbes in Allergy Committee of the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol. 2020;145(5):1332–44. https://doi.org/10.1016/j.jaci.2019.12.904.CrossRefPubMed

17.

Lukacs NW, Huang YJ. Microbiota-immune interactions in asthma pathogenesis and phenotype. Curr Opin Immunol. 2020;66:22–6. https://doi.org/10.1016/j.coi.2020.03.012.CrossRefPubMed

18.

Choi Y, Park H, Park HS, Kim YK. Extracellular vesicles, a key mediator to link environmental microbiota to airway immunity. Allergy Asthma Immunol Res. 2017;9(2):101–6. https://doi.org/10.4168/aair.2017.9.2.101.CrossRefPubMed

19.

Lambrecht BN, Hammad H. The airway epithelium in asthma. Nat Med. 2012;18(5):684–92. https://doi.org/10.1038/nm.2737.CrossRefPubMed

20.

Eisele NA, Anderson DM. Host defense and the airway epithelium: frontline responses that protect against bacterial invasion and pneumonia. J Pathog. 2011;2011:249802. https://doi.org/10.4061/2011/249802.CrossRefPubMedPubMedCentral

21.

• Hartl D, Griese M. Surfactant protein D in human lung diseases. Eur J Clin Invest. 2006;36(6):423–35. https://doi.org/10.1111/j.1365-2362.2006.01648.x This article showed changes in surfactant protein levels in patients with multiple lung diseases compared with control subjects.CrossRefPubMed

22.

Choi Y, Lee DH, Lee JH, Shin YS, Kim SH, Park HS. Immunomodulatory function of surfactant protein D in eosinophilic asthma. Allergy. 2019;74(1):192–5. https://doi.org/10.1111/all.13588.CrossRefPubMed

23.

Choi Y, Lee Y, Park HS. Which factors associated with activated eosinophils contribute to the pathogenesis of aspirin-exacerbated respiratory disease? Allergy Asthma Immunol Res. 2019;11(3):320–9. https://doi.org/10.4168/aair.2019.11.3.320.CrossRefPubMed

24.

Lopez-Rodriguez E, Gay-Jordi G, Mucci A, Lachmann N, Serrano-Mollar A. Lung surfactant metabolism: early in life, early in disease and target in cell therapy. Cell Tissue Res. 2017;367(3):721–35. https://doi.org/10.1007/s00441-016-2520-9.CrossRefPubMed

25.

Haller T, Ortmayr J, Friedrich F, Volkl H, Dietl P. Dynamics of surfactant release in alveolar type II cells. Proc Natl Acad Sci U S A. 1998;95(4):1579–84. https://doi.org/10.1073/pnas.95.4.1579.CrossRefPubMedPubMedCentral

26.

Haller T, Dietl P, Pfaller K, Frick M, Mair N, Paulmichl M, et al. Fusion pore expansion is a slow, discontinuous, and Ca2 +-dependent process regulating secretion from alveolar type II cells. J Cell Biol. 2001;155(2):279–89. https://doi.org/10.1083/jcb.200102106.CrossRefPubMedPubMedCentral

27.

Nkadi PO, Merritt TA, Pillers DA. An overview of pulmonary surfactant in the neonate: genetics, metabolism, and the role of surfactant in health and disease. Mol Genet Metab. 2009;97(2):95–101. https://doi.org/10.1016/j.ymgme.2009.01.015.CrossRefPubMedPubMedCentral

28.

Haagsman HP, Diemel RV. Surfactant-associated proteins: functions and structural variation. Comp Biochem Physiol A Mol Integr Physiol. 2001;129(1):91–108. https://doi.org/10.1016/s1095-6433(01)00308-7.CrossRefPubMed

29.

Crouch EC. Collectins and pulmonary host defense. Am J Respir Cell Mol Biol. 1998;19(2):177–201. https://doi.org/10.1165/ajrcmb.19.2.140.CrossRefPubMed

30.

Vieira F, Kung JW, 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. https://doi.org/10.1016/j.aanat.2017.03.002.CrossRefPubMedPubMedCentral

31.

Schicht M, Rausch F, Finotto S, Mathews M, Mattil A, Schubert M, et al. SFTA3, a novel protein of the lung: three-dimensional structure, characterisation and immune activation. Eur Respir J. 2014;44(2):447–56. https://doi.org/10.1183/09031936.00179813.CrossRefPubMed

32.

Weaver TE. Synthesis, processing and secretion of surfactant proteins B and C. Biochim Biophys Acta. 1998;1408(2–3):173–9. https://doi.org/10.1016/s0925-4439(98)00066-0.CrossRefPubMed

33.

Nogee LM. Genetic causes of surfactant protein abnormalities. Curr Opin Pediatr. 2019;31(3):330–9. https://doi.org/10.1097/MOP.0000000000000751.CrossRefPubMedPubMedCentral

34.

Crouch E, Persson A, Chang D, Heuser J. Molecular structure of pulmonary surfactant protein D (SP-D). J Biol Chem. 1994;269(25):17311–9.PubMed

35.

Crouch E, Wright JR. Surfactant proteins a and d and pulmonary host defense. Annu Rev. Physiol. 2001;63:521–54. https://doi.org/10.1146/annurev.physiol.63.1.521.CrossRefPubMed

36.

Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53. https://doi.org/10.1038/ni.3123.CrossRefPubMedPubMedCentral

37.

Finn PW, Bigby TD. Innate immunity and asthma. Proc Am Thorac Soc. 2009;6(3):260–5. https://doi.org/10.1513/pats.200807-064RM.CrossRefPubMedPubMedCentral

38.

Brinker KG, Garner H, Wright JR. Surfactant protein A modulates the differentiation of murine bone marrow-derived dendritic cells. Am J Physiol Lung Cell Mol Physiol. 2003;284(1):L232–41. https://doi.org/10.1152/ajplung.00187.2002.CrossRefPubMed

39.

Brandt EB, Mingler MK, Stevenson MD, Wang N, Khurana Hershey GK, Whitsett JA, et al. Surfactant protein D alters allergic lung responses in mice and human subjects. J Allergy Clin Immunol. 2008;121(5):1140–7 e2. https://doi.org/10.1016/j.jaci.2008.02.011.CrossRefPubMedPubMedCentral

40.

Oliver BG, Robinson P, Peters M, Black J. Viral infections and asthma: an inflammatory interface? Eur Respir J. 2014;44(6):1666–81. https://doi.org/10.1183/09031936.00047714.CrossRefPubMed

41.

Kim CK, Callaway Z, Gern JE. Viral infections and associated factors that promote acute exacerbations of asthma. Allergy Asthma Immunol Res. 2018;10(1):12–7. https://doi.org/10.4168/aair.2018.10.1.12.CrossRefPubMed

42.

•• Wang J, Li P, Yu Y, Fu Y, Jiang H, Lu M, et al. Pulmonary surfactant-biomimetic nanoparticles potentiate heterosubtypic influenza immunity. Science. 2020;367(6480). https://doi.org/10.1126/science.aau0810 This article highlighted the development of pulmonary surfactant-biomimetic liposomes to effectively avert exaggerated inflammation in the lung.

43.

Tan KS, Lim RL, Liu J, Ong HH, Tan VJ, Lim HF, et al. Respiratory viral infections in exacerbation of chronic airway inflammatory diseases: novel mechanisms and insights from the upper airway epithelium. Front Cell Dev Biol. 2020;8:99. https://doi.org/10.3389/fcell.2020.00099.CrossRefPubMedPubMedCentral

44.

Leth-Larsen R, Zhong F, Chow VT, Holmskov U, Lu J. The SARS coronavirus spike glycoprotein is selectively recognized by lung surfactant protein D and activates macrophages. Immunobiology. 2007;212(3):201–11. https://doi.org/10.1016/j.imbio.2006.12.001.CrossRefPubMedPubMedCentral

45.

Kloepfer KM, Lee WM, Pappas TE, Kang TJ, Vrtis RF, Evans MD et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. J Allergy Clin Immunol. 2014;133(5):1301–1307, 7 e1–3. doi:https://doi.org/10.1016/j.jaci.2014.02.030.

46.

van de Wetering JK, van Eijk M, van Golde LM, Hartung T, van Strijp JA, Batenburg JJ. Characteristics of surfactant protein A and D binding to lipoteichoic acid and peptidoglycan, 2 major cell wall components of gram-positive bacteria. J Infect Dis. 2001;184(9):1143–51. https://doi.org/10.1086/323746.CrossRefPubMed

47.

Ujma S, Horsnell WG, Katz AA, Clark HW, Schafer G. Non-pulmonary immune functions of surfactant proteins A and D. J Innate Immun. 2017;9(1):3–11. https://doi.org/10.1159/000451026.CrossRefPubMed

48.

Denning DW, O’Driscoll BR, Hogaboam CM, Bowyer P, Niven RM. The link between fungi and severe asthma: a summary of the evidence. Eur Respir J. 2006;27(3):615–26. https://doi.org/10.1183/09031936.06.00074705.CrossRefPubMed

49.

Knutsen AP, Slavin RG. Allergic bronchopulmonary aspergillosis in asthma and cystic fibrosis. Clin Dev Immunol. 2011;2011:843763. https://doi.org/10.1155/2011/843763.CrossRefPubMedPubMedCentral

50.

Madan T, Reid KB, Singh M, Sarma PU, Kishore U. Susceptibility of mice genetically deficient in the surfactant protein (SP)-A or SP-D gene to pulmonary hypersensitivity induced by antigens and allergens of Aspergillus fumigatus. J Immunol. 2005;174(11):6943–54. https://doi.org/10.4049/jimmunol.174.11.6943.CrossRefPubMed

51.

Madan T, Reid KB, Clark H, Singh M, Nayak A, Sarma PU, et al. Susceptibility of mice genetically deficient in SP-A or SP-D gene to invasive pulmonary aspergillosis. Mol Immunol. 2010;47(10):1923–30. https://doi.org/10.1016/j.molimm.2010.02.027.CrossRefPubMed

52.

Ordonez SR, van Eijk M, Escobar Salazar N, de Cock H, Veldhuizen EJA, Haagsman HP. Antifungal activities of surfactant protein D in an environment closely mimicking the lung lining. Mol Immunol. 2019;105:260–9. https://doi.org/10.1016/j.molimm.2018.12.003.CrossRefPubMed

53.

Schleich FN, Chevremont A, Paulus V, Henket M, Manise M, Seidel L, et al. Importance of concomitant local and systemic eosinophilia in uncontrolled asthma. Eur Respir J. 2014;44(1):97–108. https://doi.org/10.1183/09031936.00201813.CrossRefPubMed

54.

Cheng G, Ueda T, Nakajima H, Nakajima A, Kinjyo S, Motojima S, et al. Suppressive effects of SP-A on ionomycin-induced IL-8 production and release by eosinophils. Int Arch Allergy Immunol. 1998;117(Suppl 1):59–62. https://doi.org/10.1159/000053574.CrossRefPubMed

55.

Choi Y, Le Pham D, Lee DH, Lee SH, Kim SH, Park HS. Biological function of eosinophil extracellular traps in patients with severe eosinophilic asthma. Exp Mol Med. 2018;50(8):104. https://doi.org/10.1038/s12276-018-0136-8.CrossRefPubMedPubMedCentral

56.

Choi Y, Kim YM, Lee HR, Mun J, Sim S, Lee DH, et al. Eosinophil extracellular traps activate type 2 innate lymphoid cells through stimulating airway epithelium in severe asthma. Allergy. 2020;75(1):95–103. https://doi.org/10.1111/all.13997.CrossRefPubMed

57.

Lee Y, Lee JH, Yang EM, Kwon E, Jung CG, Kim SC, et al. Serum levels of eosinophil-derived neurotoxin: a biomarker for asthma severity in adult asthmatics. Allergy Asthma Immunol Res. 2019;11(3):394–405. https://doi.org/10.4168/aair.2019.11.3.394.CrossRefPubMedPubMedCentral

58.

Yousefi S, Sharma SK, Stojkov D, Germic N, Aeschlimann S, Ge MQ, et al. Oxidative damage of SP-D abolishes control of eosinophil extracellular DNA trap formation. J Leukoc Biol. 2018;104(1):205–14. https://doi.org/10.1002/JLB.3AB1117-455R.CrossRefPubMedPubMedCentral

59.

• Choi Y, Lee DH, Trinh HKT, Ban GY, Park HK, Shin YS, et al. Surfactant protein D alleviates eosinophil-mediated airway inflammation and remodeling in patients with aspirin-exacerbated respiratory disease. Allergy. 2019;74(1):78–88. https://doi.org/10.1111/all.13458 This article suggested a possible approach for enhancing surfactant protein expression in airway epithelial cells.CrossRefPubMed

60.

Pelaia C, Paoletti G, Puggioni F, Racca F, Pelaia G, Canonica GW, et al. Interleukin-5 in the pathophysiology of severe asthma. Front Physiol. 2019;10:1514. https://doi.org/10.3389/fphys.2019.01514.CrossRefPubMedPubMedCentral

61.

Pastva AM, Wright JR, Williams KL. Immunomodulatory roles of surfactant proteins A and D: implications in lung disease. Proc Am Thorac Soc. 2007;4(3):252–7. https://doi.org/10.1513/pats.200701-018AW.CrossRefPubMedPubMedCentral

62.

Borron P, Veldhuizen RA, Lewis JF, Possmayer F, Caveney A, Inchley K, et al. Surfactant associated protein-A inhibits human lymphocyte proliferation and IL-2 production. Am J Respir Cell Mol Biol. 1996;15(1):115–21. https://doi.org/10.1165/ajrcmb.15.1.8679215.CrossRefPubMed

63.

Borron PJ, Crouch EC, Lewis JF, Wright JR, Possmayer F, Fraher LJ. Recombinant rat surfactant-associated protein D inhibits human T lymphocyte proliferation and IL-2 production. J Immunol. 1998;161(9):4599–603.PubMed

64.

Nag S, Lamkhioued B, Renzi PM. Interleukin-2-induced increased airway responsiveness and lung Th2 cytokine expression occur after antigen challenge through the leukotriene pathway. Am J Respir Crit Care Med. 2002;165(11):1540–5. https://doi.org/10.1164/rccm.2109012.CrossRefPubMed

65.

Francisco D, Wang Y, Conway M, Hurbon AN, Dy ABC, Addison KJ, et al. Surfactant protein-A protects against IL-13-induced inflammation in asthma. J Immunol. 2020;204(10):2829–39. https://doi.org/10.4049/jimmunol.1901227.CrossRefPubMed

66.

Schaub B, Westlake RM, He H, Arestides R, Haley KJ, Campo M, et al. Surfactant protein D deficiency influences allergic immune responses. Clin Exp Allergy. 2004;34(12):1819–26. https://doi.org/10.1111/j.1365-2222.2004.02068.x.CrossRefPubMed

67.

Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, et al. Interleukin-13: central mediator of allergic asthma. Science. 1998;282(5397):2258–61. https://doi.org/10.1126/science.282.5397.2258.CrossRefPubMed

68.

Wang JY, Kishore U, Lim BL, Strong P, Reid KB. Interaction of human lung surfactant proteins A and D with mite (Dermatophagoides pteronyssinus) allergens. Clin Exp Immunol. 1996;106(2):367–73. https://doi.org/10.1046/j.1365-2249.1996.d01-838.x.CrossRefPubMedPubMedCentral

69.

Hentschel R, Bohlin K, van Kaam A, Fuchs H, Danhaive O. Surfactant replacement therapy: from biological basis to current clinical practice. Pediatr Res. 2020. https://doi.org/10.1038/s41390-020-0750-8.

70.

Raghavendran K, Willson D, Notter RH. Surfactant therapy for acute lung injury and acute respiratory distress syndrome. Crit Care Clin. 2011;27(3):525–59. https://doi.org/10.1016/j.ccc.2011.04.005.CrossRefPubMedPubMedCentral

71.

Willson DF, Notter RH. The future of exogenous surfactant therapy. Respir Care. 2011;56(9):1369–86; discussion 86–8. https://doi.org/10.4187/respcare.01306.CrossRefPubMed

72.

Sweet DG, Turner MA, Stranak Z, Plavka R, Clarke P, Stenson BJ, et al. A first-in-human clinical study of a new SP-B and SP-C enriched synthetic surfactant (CHF5633) in preterm babies with respiratory distress syndrome. Arch Dis Child Fetal Neonatal Ed. 2017;102(6):F497–503. https://doi.org/10.1136/archdischild-2017-312,722.CrossRefPubMedPubMedCentral

73.

Madsen J, Panchal MH, Mackay RA, Echaide M, Koster G, Aquino G, et al. Metabolism of a synthetic compared with a natural therapeutic pulmonary surfactant in adult mice. J Lipid Res. 2018;59(10):1880–92. https://doi.org/10.1194/jlr.M085431.CrossRefPubMedPubMedCentral

74.

Gladstone IM, Mercurio MR, Devenny SG, Jacobs HC. Antenatal steroids, postnatal surfactant, and pulmonary function in premature rabbits. J Appl Physiol (1985). 1989;67(4):1377–82. https://doi.org/10.1152/jappl.1989.67.4.1377.CrossRef

75.

Kamio K, Usuki J, Azuma A, Matsuda K, Ishii T, Inomata M, et al. Nintedanib modulates surfactant protein-D expression in A549 human lung epithelial cells via the c-Jun N-terminal kinase-activator protein-1 pathway. Pulm Pharmacol Ther. 2015;32:29–36. https://doi.org/10.1016/j.pupt.2015.03.001.CrossRefPubMed

76.

Cheng G, Ueda T, Numao T, Kuroki Y, Nakajima H, Fukushima Y, et al. Increased levels of surfactant protein A and D in bronchoalveolar lavage fluids in patients with bronchial asthma. Eur Respir J. 2000;16(5):831–5. https://doi.org/10.1183/09031936.00.16583100.CrossRefPubMed

77.

Okazaki S, Murai H, Kidoguchi S, Nomura E, Itoh N, Hashimoto N, et al. The biomarker salivary SP-D may indicate small airway inflammation and asthma exacerbation. J Investig Allergol Clin Immunol. 2017;27(5):305–12. https://doi.org/10.18176/jiaci.0174.CrossRefPubMed

78.

Fakih D, Akiki Z, Junker K, Medlej-Hashim M, Waked M, Salameh P, et al. Surfactant protein D multimerization and gene polymorphism in COPD and asthma. Respirology. 2018;23(3):298–305. https://doi.org/10.1111/resp.13193.CrossRefPubMed

79.

Koopmans JG, van der Zee JS, Krop EJ, Lopuhaa CE, Jansen HM, Batenburg JJ. Serum surfactant protein D is elevated in allergic patients. Clin Exp Allergy. 2004;34(12):1827–33. https://doi.org/10.1111/j.1365-2222.2004.02083.x.CrossRefPubMed

80.

Xu J, Singhera GK, Dorscheid DR. Expression of surfactant protein D in airways of asthmatics and interleukin-13 modulation of surfactant protein D in human models of airway epithelium. Respir Res. 2015;16:26. https://doi.org/10.1186/s12931-015-0177-7.CrossRefPubMedPubMedCentral

81.

• Mackay RM, Grainge CL, Lau LC, Barber C, Clark HW, Howarth PH. Airway surfactant protein D deficiency in adults with severe asthma. Chest. 2016;149(5):1165–72. https://doi.org/10.1016/j.chest.2015.11.012 This article revealed deficiency of surfactant proteins in severe asthma increased epithelial damage and permeability within the peripheral airways.CrossRefPubMedPubMedCentral

82.

Emmanouil P, Loukides S, Kostikas K, Papatheodorou G, Papaporfyriou A, Hillas G, et al. Sputum and BAL Clara cell secretory protein and surfactant protein D levels in asthma. Allergy. 2015;70(6):711–4. https://doi.org/10.1111/all.12603.CrossRefPubMed

83.

Benfante A, Battaglia S, Principe S, Di Mitri C, Paterno A, Spatafora M, et al. Asthmatics with high levels of serum surfactant protein D have more severe disease. Eur Respir J. 2016;47(6):1864–7. https://doi.org/10.1183/13993003.02142-2015.CrossRefPubMed

84.

Lugogo N, Francisco D, Addison KJ, Manne A, Pederson W, Ingram JL, et al. Obese asthmatic patients have decreased surfactant protein A levels: mechanisms and implications. J Allergy Clin Immunol. 2018;141(3):918–26 e3. https://doi.org/10.1016/j.jaci.2017.05.028.CrossRefPubMed

Title: Pulmonary Surfactants: a New Therapeutic Target in Asthma
Authors: Youngwoo Choi
Jaehyuk Jang
Hae-Sim Park
Publication date: 01-11-2020
Publisher: Springer US
Keywords: Bronchial Asthma
Acute Respiratory Distress-Syndrome
Published in: Current Allergy and Asthma Reports / Issue 11/2020
Print ISSN: 1529-7322
Electronic ISSN: 1534-6315
DOI: https://doi.org/10.1007/s11882-020-00968-8

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Pulmonary Surfactants: a New Therapeutic Target in Asthma

Abstract

Purpose of Review

Recent Findings

Summary

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose of Review

Recent Findings

Summary

Please log in to get access to this content

Other articles of this Issue 11/2020

The Child with Elevated IgE and Infection Susceptibility

Asking the Right Questions—Human Factors Considerations for Telemedicine Design

Clinical Evidence and Biomarkers Linking Allergy and Acute or Chronic Rhinosinusitis in Children: a Systematic Review

Traditional Chinese Medicine (TCM) and Allergic Diseases

Safety of Intranasal Steroids: an Updated Perspective

Correction to: Alpha-1 Antitrypsin Deficiency: a Rare Disease?