Surfactant and its role in the pathobiology of pulmonary infection

Microbes and Infection

Volumn 14, Issue 1, 2012, Pages 17-25

  Glasser, Jennifer R ^a   Mallampalli, Rama K ^a,b,c  

^a Acute Lung Injury Center of Excellence   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Veteran Affairs Pittsburgh Health Care System   (United States)

Author keywords

Collectin; Infection; Phospholipid; Surfactant

Indexed keywords

COLLECTIN; LIPID; LUNG SURFACTANT; PHOSPHOLIPID; SURFACTANT PROTEIN A; SURFACTANT PROTEIN B; SURFACTANT PROTEIN C; SURFACTANT PROTEIN D;

BACTERIUM; FUNGUS; HOMEOSTASIS; HOST CELL; HUMAN; HYDROPHOBICITY; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LUNG INFECTION; MYCOPLASMA; NONHUMAN; PATHOGENESIS; PATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; SHORT SURVEY; VIRUS; VIRUS INFECTION; YEAST;

ANIMALS; COMMUNICABLE DISEASES; HUMANS; IMMUNOLOGIC FACTORS; LUNG DISEASES; PULMONARY SURFACTANTS;

EID: 84355162144     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.08.019     Document Type: Short Survey

References (67)

1. Mulugeta S., Beers M.F. Surfactant protein C: its unique properties and emerging immunomodulatory role in the lung. Microbes Infect. 2006, 8:2317-2323.
2. Orgeig S., Hiemstra P.S., Veldhuizen E.J., Casals C., Clark H.W., Haczku A., Knudsen L., Possmayer F. Recent advances in alveolar biology: evolution and function of alveolar proteins. Respir. Physiol. Neurobiol. 2010, 173(Suppl.):S43-S54.
3. Maina J.N., West J.B., Orgeig S., Foot N.J., Daniels C.B., Kiama S.G., Gehr P., Muhlfeld C., Blank F., Muller L., Lehmann A., Brandenberger C., Rothen-Rutishauser B. Recent advances into understanding some aspects of the structure and function of mammalian and avian lungs. Physiol. Biochem. Zool. 2010, 83:792-807.
4. Rooney S.A., Young S.L., Mendelson C.R. Molecular and cellular processing of lung surfactant. FASEB J. 1994, 8:957-967.
5. Schmidt R., Markart P., Ruppert C., Wygrecka M., Kuchenbuch T., Walmrath D., Seeger W., Guenther A. Time-dependent changes in pulmonary surfactant function and composition in acute respiratory distress syndrome due to pneumonia or aspiration. Respir. Res. 2007, 8:55.
6. Barreira E.R., Precioso A.R., Bousso A. Pulmonary surfactant in respiratory syncytial virus bronchiolitis: the role in pathogenesis and clinical implications. Pediatr. Pulmonol. 2010.
7. Mingarro I., Lukovic D., Vilar M., Perez-Gil J. Synthetic pulmonary surfactant preparations: new developments and future trends. Curr. Med. Chem. 2008, 15:393-403.
8. Blanco O., Perez-Gil J. Biochemical and pharmacological differences between preparations of exogenous natural surfactant used to treat respiratory distress syndrome: role of the different components in an efficient pulmonary surfactant. Eur. J. Pharmacol. 2007, 568:1-15.
9. Pace P.W., Yao L.J., Wilson J.X., Possmayer F., Veldhuizen R.A., Lewis J.F. The effects of hyperoxia exposure on lung function and pulmonary surfactant in a rat model of acute lung injury. Exp. Lung Res. 2009, 35:380-398.
10. Maruscak A.A., Vockeroth D.W., Girardi B., Sheikh T., Possmayer F., Lewis J.F., Veldhuizen R.A. Alterations to surfactant precede physiological deterioration during high tidal volume ventilation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L974-L983.
11. Veldhuizen R., Nag K., Orgeig S., Possmayer F. The role of lipids in pulmonary surfactant. Biochim. Biophys. Acta 1998, 1408:90-108.
12. Hohlfeld J., Fabel H., Hamm H. The role of pulmonary surfactant in obstructive airways disease. Eur. Respir. J. 1997, 10:482-491.
13. LeVine A.M., Whitsett J.A. Pulmonary collectins and innate host defense of the lung. Microbes Infect. 2001, 3:161-166.
14. Kingma P.S., Whitsett J.A. In defense of the lung: surfactant protein A and surfactant protein D. Curr. Opin. Pharmacol. 2006, 6:277-283.
15. Ledford J.G., Pastva A.M., Wright J.R. Review: collectins link innate and adaptive immunity in allergic airway disease. Innate Immun. 2010, 16:183-190.
16. Haagsman H.P., Hogenkamp A., van Eijk M., Veldhuizen E.J. Surfactant collectins and innate immunity. Neonatology 2008, 93:288-294.
17. Markart P., Ruppert C., Wygrecka M., Colaris T., Dahal B., Walmrath D., Harbach H., Wilhelm J., Seeger W., Schmidt R., Guenther A. Patients with ARDS show improvement but not normalisation of alveolar surface activity with surfactant treatment: putative role of neutral lipids. Thorax 2007, 62:588-594.
18. Gomez-Gil L., Schurch D., Goormaghtigh E., Perez-Gil J. Pulmonary surfactant protein SP-C counteracts the deleterious effects of cholesterol on the activity of surfactant films under physiologically relevant compression-expansion dynamics. Biophys. J. 2009, 97:2736-2745.
19. Picardi M.V., Cruz A., Orellana G., Perez-Gil J. Phospholipid packing and hydration in pulmonary surfactant membranes and films as sensed by LAURDAN. Biochim. Biophys. Acta 2011, 1808:696-705.
20. Schurch D., Ospina O.L., Cruz A., Perez-Gil J. Combined and independent action of proteins SP-B and SP-C in the surface behavior and mechanical stability of pulmonary surfactant films. Biophys. J. 2010, 99:3290-3299.
21. Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim. Biophys. Acta 1998, 1408:79-89.
22. Muhlfeld C., Becker L., Bussinger C., Vollroth M., Nagib R., Schaefer I.M., Knudsen L., Richter J., Madershahian N., Wahlers T., Wittwer T., Ochs M. Exogenous surfactant in ischemia/reperfusion: effects on endogenous surfactant pools. J. Heart Lung Transplant 2010, 29:327-334.
23. O'Reilly M.A., Nogee L., Whitsett J.A. Requirement of the collagenous domain for carbohydrate processing and secretion of a surfactant protein, SP-A. Biochim. Biophys. Acta 1988, 969:176-184.
24. Ballard P.L. Hormones and lung maturation. Monogr. Endocrinol. 1986, 28:1-354.
25. Postle A.D., Gonzales L.W., Bernhard W., Clark G.T., Godinez M.H., Godinez R.I., Ballard P.L. Lipidomics of cellular and secreted phospholipids from differentiated human fetal type II alveolar epithelial cells. J. Lipid Res. 2006, 47:1322-1331.
26. Curstedt T., Johansson J. Different effects of surfactant proteins B and C - implications for development of synthetic surfactants. Neonatology 2010, 97:367-372.
27. Gakhar L., Bartlett J.A., Penterman J., Mizrachi D., Singh P.K., Mallampalli R.K., Ramaswamy S., McCray P.B. PLUNC is a novel airway surfactant protein with anti-biofilm activity. PLoS One 2010, 5:e9098.
28. Garcia-Verdugo I., Garcia de Paco E., Espinassous Q., Gonzalez-Horta A., Synguelakis M., Kanellopoulos J., Rivas L., Chaby R., Perez-Gil J. Synthetic peptides representing the N-terminal segment of surfactant protein C modulate LPS-stimulated TNF-alpha production by macrophages. Innate Immun. 2009, 15:53-62.
29. Cameron H.S., Somaschini M., Carrera P., Hamvas A., Whitsett J.A., Wert S.E., Deutsch G., Nogee L.M. A common mutation in the surfactant protein C gene associated with lung disease. J. Pediatr. 2005, 146:370-375.
30. Lawson W.E., Polosukhin V.V., Stathopoulos G.T., Zoia O., Han W., Lane K.B., Li B., Donnelly E.F., Holburn G.E., Lewis K.G., Collins R.D., Hull W.M., Glasser S.W., Whitsett J.A., Blackwell T.S. Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am. J. Pathol. 2005, 167:1267-1277.
31. Hickman-Davis J.M., Fang F.C., Nathan C., Shepherd V.L., Voelker D.R., Wright J.R. Lung surfactant and reactive oxygen-nitrogen species: antimicrobial activity and host-pathogen interactions. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 281:L517-L523.
32. Mason R.J., Greene K., Voelker D.R. Surfactant protein A and surfactant protein D in health and disease. Am. J. Physiol. 1998, 275:L1-L13.
33. Alcorn J.F., Wright J.R. Degradation of pulmonary surfactant protein D by Pseudomonas aeruginosa elastase abrogates innate immune function. J. Biol. Chem. 2004, 279:30871-30879.
34. Shang F., Rynkiewicz M.J., McCormack F.X., Wu H., Cafarella T.M., Head J.F., Seaton B.A. Crystallographic complexes of surfactant protein A and carbohydrates reveal ligand-induced conformational change. J. Biol. Chem. 2011, 286:757-765.
35. Kishore U., Greenhough T.J., Waters P., Shrive A.K., Ghai R., Kamran M.F., Bernal A.L., Reid K.B., Madan T., Chakraborty T. Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol. Immunol. 2006, 43:1293-1315.
36. Sever-Chroneos Z., Krupa A., Davis J., Hasan M., Yang C.H., Szeliga J., Herrmann M., Hussain M., Geisbrecht B.V., Kobzik L., Chroneos Z.C. 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. 2011, 286:4854-4870.
37. Kuang Z., Hao Y., Hwang S., Zhang S., Kim E., Akinbi H.T., Schurr M.J., Irvin R.T., Hassett D.J., Lau G.W. The Pseudomonas aeruginosa flagellum confers resistance to pulmonary surfactant protein-A by impacting the production of exoproteases through quorum-sensing. Mol. Microbiol. 2011, 79:1220-1235.
38. Chiba H., Pattanajitvilai S., Mitsuzawa H., Kuroki Y., Evans A., Voelker D.R. Pulmonary surfactant proteins A and D recognize lipid ligands on Mycoplasma pneumoniae and markedly augment the innate immune response to the organism. Chest 2003, 123:426S.
39. Qi L., Kash J.C., Dugan V.G., Jagger B.W., Lau Y.F., Sheng Z.M., Crouch E.C., Hartshorn K.L., Taubenberger J.K. The ability of pandemic influenza virus hemagglutinins to induce lower respiratory pathology is associated with decreased surfactant protein D binding. Virology 2011, 412:426-434.
40. Floros J., Wang Guirong, Mikerov Anatoly N. Genetic complexity of the human innate host defense molecules, surfactant protein A1 (SP-A1) and SP-A2-impact on function. Crit. Rev. Eukaryot. Gene Expr. 2009, 19:125-137.
41. Jakel A., Clark H., Reid K.B., Sim R.B. Surface-bound myeloperoxidase is a ligand for recognition of late apoptotic neutrophils by human lung surfactant proteins A and D. Protein Cell 2010, 1:563-572.
42. Litvack M.L., Djiadeu P., Renganathan S.D., Sy S., Post M., Palaniyar N. Natural IgM and innate immune collectin SP-D bind to late apoptotic cells and enhance their clearance by alveolar macrophages in vivo. Mol. Immunol. 2010, 48:37-47.
43. Guo C.J., Atochina-Vasserman E.N., Abramova E., Foley J.P., Zaman A., Crouch E., Beers M.F., Savani R.C., Gow A.J. S-Nitrosylation of surfactant protein-D controls inflammatory function. PLoS Biol. 2008, 6:e266.
44. Kazi A.S., Tao J.Q., Feinstein S.I., Zhang L., Fisher A.B., Bates S.R. Role of the PI3-kinase signaling pathway in trafficking of the surfactant protein A receptor P63 (CKAP4) on type II pneumocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 299:L794-L807.
45. White M.K., Strayer D.S. Survival signaling in type II pneumocytes activated by surfactant protein-A. Exp. Cell Res. 2002, 280:270-279.
46. Henning L.N., Azad A.K., Parsa K.V., Crowther J.E., Tridandapani S., Schlesinger L.S. Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J. Immunol. 2008, 180:7847-7858.
47. Mander A., Langton-Hewer S., Bernhard W., Warner J.O., Postle A.D. Altered phospholipid composition and aggregate structure of lung surfactant is associated with impaired lung function in young children with respiratory infections. Am. J. Respir. Cell Mol. Biol. 2002, 27:714-721.
48. Chao W., Spragg R.G., Smith R.M. Inhibitory effect of porcine surfactant on the respiratory burst oxidase in human neutrophils. Attenuation of p47phox and p67phox membrane translocation as the mechanism. J. Clin. Invest. 1995, 96:2654-2660.
49. Kuronuma K., Mitsuzawa H., Takeda K., Nishitani C., Chan E.D., Kuroki Y., Nakamura M., Voelker D.R. Anionic pulmonary surfactant phospholipids inhibit inflammatory responses from alveolar macrophages and U937 cells by binding the lipopolysaccharide-interacting proteins CD14 and MD-2. J. Biol. Chem. 2009, 284:25488-25500.
50. Numata M., Chu H.W., Dakhama A., Voelker D.R. Pulmonary surfactant phosphatidylglycerol inhibits respiratory syncytial virus-induced inflammation and infection. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:320-325.
51. Ray N.B., Durairaj L., Chen B.B., McVerry B.J., Ryan A.J., Donahoe M., Waltenbaugh A.K., O'Donnell C.P., Henderson F.C., Etscheidt C.A., McCoy D.M., Agassandian M., Hayes-Rowan E.C., Coon T.A., Butler P.L., Gakhar L., Mathur S.N., Sieren J.C., Tyurina Y.Y., Kagan V.E., McLennan G., Mallampalli R.K. Dynamic regulation of cardiolipin by the lipid pump Atp8b1 determines the severity of lung injury in experimental pneumonia. Nat. Med. 2010, 16:1120-1127.
52. Perino J., Crouzier D., Spehner D., Debouzy J.C., Garin D., Crance J.M., Favier A.L. Lung surfactant DPPG phospholipid inhibits vaccinia virus infection. Antivir. Res. 2011, 89:89-97.
53. Balakireva L., Schoehn G., Thouvenin E., Chroboczek J. Binding of adenovirus capsid to dipalmitoyl phosphatidylcholine provides a novel pathway for virus entry. J. Virol. 2003, 77:4858-4866.
54. Coil D.A., Miller A.D. Enhancement of enveloped virus entry by phosphatidylserine. J. Virol. 2005, 79:11496-11500.
55. Mercer J., Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320:531-535.
56. Laliberte J.P., Moss B. Appraising the apoptotic mimicry model and the role of phospholipids for poxvirus entry. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17517-17521.
57. Mariencheck W.I., Alcorn J.F., Palmer S.M., Wright J.R. Pseudomonas aeruginosa elastase degrades surfactant proteins A and D. Am. J. Respir. Cell Mol. Biol. 2003, 28:528-537.
58. Malloy J.L., Veldhuizen R.A., Thibodeaux B.A., O'Callaghan R.J., Wright J.R. Pseudomonas aeruginosa protease IV degrades surfactant proteins and inhibits surfactant host defense and biophysical functions. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 288:L409-L418.
59. Wu Y., Xu Z., Henderson F.C., Ryan A.J., Yahr T.L., Mallampalli R.K. Chronic Pseudomonas aeruginosa infection reduces surfactant levels by inhibiting its biosynthesis. Cell Microbiol. 2007, 9:1062-1072.
60. Henderson F.C., Miakotina O.L., Mallampalli R.K. Proapoptotic effects of P. aeruginosa involve inhibition of surfactant phosphatidylcholine synthesis. J. Lipid Res. 2006, 47:2314-2324.
61. Miakotina O.L., McCoy D.M., Shi L., Look D.C., Mallampalli R.K. Human adenovirus modulates surfactant phospholipid trafficking. Traffic 2007, 8:1765-1777.
62. Zhou J., Wu Y., Henderson F., McCoy D.M., Salome R.G., McGowan S.E., Mallampalli R.K. Adenoviral gene transfer of a mutant surfactant enzyme ameliorates Pseudomonas-induced lung injury. Gene Ther. 2006, 13:974-985.
63. Pankhaniya R.R., Tamura M., Allmond L.R., Moriyama K., Ajayi T., Wiener-Kronish J.P., Sawa T. Pseudomonas aeruginosa causes acute lung injury via the catalytic activity of the patatin-like phospholipase domain of ExoU. Crit. Care Med. 2004, 32:2293-2299.
64. Attalah H.L., Wu Y., Alaoui-El-Azher M., Thouron F., Koumanov K., Wolf C., Brochard L., Harf A., Delclaux C., Touqui L. Induction of type-IIA secretory phospholipase A2 in animal models of acute lung injury. Eur. Respir. J. 2003, 21:1040-1045.
65. Kawasaki Y., Endo K., Suyama K., Sato M., Ito M., Hashimoto K., Hosoya M. Serum SP-D levels as a biomarker of lung injury in respiratory syncytial virus bronchiolitis. Pediatr. Pulmonol. 2011, 46:18-22.
66. Haczku A. Protective role of the lung collectins surfactant protein A and surfactant protein D in airway inflammation. J. Allergy Clin. Immunol. 2008, 122:861-879. (quiz 880-861).
67. Forbes L.R., Haczku A. SP-D and regulation of the pulmonary innate immune system in allergic airway changes. Clin. Exp. Allergy 2010, 40:547-562.