Structural Features Essential to the Antimicrobial Functions of Human SPLUNC1

Biochemistry

Volumn 55, Issue 21, 2016, Pages 2979-2991

  Walton, William G ^a   Ahmad, Saira ^b   Little, Michael S ^a   Kim, Christine S K ^b   Tyrrell, Jean ^b   Lin, Qiao ^c   Di, Y Peter ^c   Tarran, Robert ^b   Redinbo, Matthew R ^a  

^a The University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINS; CRYSTAL STRUCTURE; MAMMALS; MICROORGANISMS; PROTEINS; SOLID SOLUTIONS; SURFACE ACTIVE AGENTS;

ANTIMICROBIAL FUNCTIONS; BACTERIOSTATIC ACTIONS; CONFORMATIONAL FLEXIBILITY; GRAM-NEGATIVE BACTERIA; GRAM-NEGATIVE PATHOGENS; GRAM-POSITIVE BACTERIUM; PSEUDOMONAS AERUGINOSA; SURFACE ELECTROSTATICS;

BACTERIA;

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; LEUCINE; SHORT PALATE LUNG NASAL EPITHELIAL CLONE 1 PROTEIN; SURFACTANT; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BPIFA1 PROTEIN, HUMAN; GLYCOPROTEIN; LIPOPOLYSACCHARIDE; LUNG SURFACTANT; PHOSPHOPROTEIN;

ARTICLE; BURKHOLDERIA CENOCEPACIA; CLINICAL FEATURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; ION EXCHANGE CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY; AMINO ACID SEQUENCE; BIOFILM; BRONCHUS; CELL CULTURE; CHEMISTRY; CRYSTALLIZATION; CYTOLOGY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; BIOFILMS; BRONCHI; BURKHOLDERIA CENOCEPACIA; CELLS, CULTURED; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; GLYCOPROTEINS; HUMANS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; PHOSPHOPROTEINS; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; PULMONARY SURFACTANTS;

EID: 84973402461     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.6b00271     Document Type: Article

References (40)

1. Bingle, C. D. and Bingle, L. (2000) Biochim. Biophys. Acta, Gene Struct. Expression 1493, 363-367 10.1016/S0167-4781(00)00196-2
2. Bingle, L. and Bingle, C. D. (2011) Distribution of human PLUNC/BPI fold-containing (BPIF) proteins Biochem. Soc. Trans. 39, 1023-1027 10.1042/BST0391023
3. Bingle, C. D., Seal, R. L., and Craven, C. J. (2011) Systematic nomenclature for the PLUNC/PSP/BSP30/SMGB proteins as a subfamily of the BPI fold-containing superfamily Biochem. Soc. Trans. 39, 977-983 10.1042/BST0390977
4. Britto, C. J. and Cohn, L. (2015) Bactericidal/Permeability-increasing protein fold-containing family member A1 in airway host protection and respiratory disease Am. J. Respir. Cell Mol. Biol. 52, 525-534 10.1165/rcmb.2014-0297RT
5. Hobbs, C. a, Blanchard, M. G., Kellenberger, S., Bencharit, S., Cao, R., Kesimer, M., Walton, W. G., Redinbo, M. R., Stutts, M. J., and Tarran, R. (2012) Identification of SPLUNC1s ENaC-inhibitory domain yields novel strategies to treat sodium hyperabsorption in cystic fibrosis airways FASEB J. 26, 4348-4359 10.1096/fj.12-207431
6. Garland, A. L., Walton, W. G., Coakley, R. D., Tan, C. D., Gilmore, R. C., Hobbs, C. A., Tripathy, A., Clunes, L. A., Bencharit, S., Stutts, M. J., Betts, L., Redinbo, M. R., and Tarran, R. (2013) Molecular basis for pH-dependent mucosal dehydration in cystic fibrosis airways Proc. Natl. Acad. Sci. U. S. A. 110, 15973-15978 10.1073/pnas.1311999110
7. Di, Y. P. (2011) Functional roles of SPLUNC1 in the innate immune response against Gram-negative bacteria Biochem. Soc. Trans. 39, 1051-1055 10.1042/BST0391051
8. Bartlett, J., Gakhar, L., Penterman, J., Singh, P., Mallampalli, R. K., Porter, E., and McCray, P. B. (2011) PLUNC: a multifunctional surfactant of the airways Biochem. Soc. Trans. 39, 1012-1016 10.1042/BST0391012
9. Chu, H. W., Thaikoottathil, J., Rino, J. G., Zhang, G., Wu, Q., Moss, T., Refaeli, Y., Bowler, R., Wenzel, S. E., Chen, Z., Zdunek, J., Breed, R., Young, R., Allaire, E., and Martin, R. J. (2007) Function and regulation of SPLUNC1 protein in Mycoplasma infection and allergic inflammation J. Immunol. 179, 3995-4002 10.4049/jimmunol.179.6.3995
10. Gakhar, L., Bartlett, J. A., Penterman, J., Mizrachi, D., Singh, P. K., Mallampalli, R. K., Ramaswamy, S., and McCray, P. B. (2010) PLUNC is a novel airway surfactant protein with anti-biofilm activity PLoS One 5, e9098 10.1371/journal.pone.0009098
11. McGillivary, G. and Bakaletz, L. O. (2010) The multifunctional host defense peptide SPLUNC1 is critical for homeostasis of the mammalian upper airway PLoS One 5, e13224 10.1371/journal.pone.0013224
12. Thaikoottathil, J. V., Martin, R. J., Di, P. Y., Minor, M., Case, S., Zhang, B., Zhang, G., Huang, H., and Chu, H. W. (2012) SPLUNC1 deficiency enhances airway eosinophilic inflammation in mice Am. J. Respir. Cell Mol. Biol. 47, 253-260 10.1165/rcmb.2012-0064OC
13. Liu, Y., Bartlett, J. a., Di, M. E., Bomberger, J. M., Chan, Y. R., Gakhar, L., Mallampalli, R. K., McCray, P. B., and Di, Y. P. (2013) SPLUNC1/BPIFA1 contributes to pulmonary host defense against klebsiella pneumoniae respiratory infection Am. J. Pathol. 182, 1519-1531 10.1016/j.ajpath.2013.01.050
14. Kohlgraf, K. G., Ackermann, A. R., Burnell, K. K., Srikantha, R. N., Joly, S. A., Bartlett, J. A., Gakhar, L., Johnson, G. K., McCray, P. B., Guthmiller, J. M., and Brogden, K. A. (2012) Quantitation of SPLUNC1 in saliva with an xMAP particle-based antibody capture and detection immunoassay Arch. Oral Biol. 57, 197-204 10.1016/j.archoralbio.2011.08.013
15. Bartlett, J. A., Meyerholz, D. K., Wohlford-Lenane, C. L., Naumann, P. W., Salzman, N. H., and McCray, P. B. (2015) Increased susceptibility to otitis media in a Splunc1-deficient mouse model Dis. Models & Mech. 8, 501-508 10.1242/dmm.019646
16. Gally, F., Di, Y. P., Smith, S. K., Minor, M. N., Liu, Y., Bratton, D. L., Frasch, S. C., Michels, N. M., Case, S. R., and Chu, H. W. (2011) SPLUNC1 promotes lung innate defense against Mycoplasma pneumoniae infection in mice Am. J. Pathol. 178, 2159-2167 10.1016/j.ajpath.2011.01.026
17. Lukinskiene, L., Liu, Y., Reynolds, S. D., Steele, C., Stripp, B. R., Leikauf, G. D., Kolls, J. K., and Di, Y. P. (2011) Antimicrobial activity of PLUNC protects against Pseudomonas aeruginosa infection J. Immunol. 187, 382-390 10.4049/jimmunol.1001769
18. Zhou, H.-D., Li, X.-L., Li, G.-Y., Zhou, M., Liu, H.-Y., Yang, Y.-X., Deng, T., Ma, J., and Sheng, S.-R. (2008) Effect of SPLUNC1 protein on the Pseudomonas aeruginosa and Epstein-Barr virus Mol. Cell. Biochem. 309, 191-197 10.1007/s11010-007-9659-3
19. Chu, H. W., Gally, F., Thaikoottathil, J., Janssen-Heininger, Y. M., Wu, Q., Zhang, G., Reisdorph, N., Case, S., Minor, M., Smith, S., Jiang, D., Michels, N., Simon, G., and Martin, R. J. (2010) SPLUNC1 regulation in airway epithelial cells: role of Toll-like receptor 2 signaling Respir Res. 11, 155 10.1186/1465-9921-11-155
20. Jiang, D., Persinger, R., Wu, Q., Gross, A., and Chu, H. W. (2013) α1-Antitrypsin promotes SPLUNC1-mediated lung defense against Pseudomonas aeruginosa infection in mice Respir. Res. 14, 122 10.1186/1465-9921-14-122
21. Liu, Y., Di, M. E., Chu, H. W., Liu, X., Wang, L., Wenzel, S., and Di, Y. P. (2013) Increased Susceptibility to Pulmonary Pseudomonas Infection in Splunc1 Knockout Mice J. Immunol. 191, 4259-4268 10.4049/jimmunol.1202340
22. Zhou, H. D., Li, G. Y., Yang, Y. X., Li, X. L., Sheng, S. R., Zhang, W. L., and Zhao, J. (2006) Intracellular co-localization of SPLUNC1 protein with nanobacteria in nasopharyngeal carcinoma epithelia HNE1 cells depended on the bactericidal permeability increasing protein domain Mol. Immunol. 43, 1864-1871 10.1016/j.molimm.2005.10.021
23. Sayeed, S., Nistico, L., St Croix, C., and Di, Y. P. (2013) Multifunctional role of human SPLUNC1 in Pseudomonas aeruginosa infection Infect. Immun. 81, 285-291 10.1128/IAI.00500-12
24. Ghafouri, B., Kihlström, E., Tagesson, C., and Lindahl, M. (2004) PLUNC in human nasal lavage fluid: multiple isoforms that bind to lipopolysaccharide Biochim. Biophys. Acta, Proteins Proteomics 1699, 57-63 10.1016/j.bbapap.2004.01.001
25. Ning, F., Wang, C., Berry, K. Z., Kandasamy, P., Liu, H., Murphy, R. C., Voelker, D. R., Nho, C. W., Pan, C.-H., Dai, S., Niu, L., Chu, H.-W., and Zhang, G. (2014) Structural characterization of the pulmonary innate immune protein SPLUNC1 and identification of lipid ligands FASEB J. 28, 5349-5360 10.1096/fj.14-259291
26. Kopec, K. O., Alva, V., and Lupas, A. N. (2011) Biochem. Soc. Trans. 39, 1033-1038 10.1042/BST0391033
27. McDonald, R. E., Fleming, R. I., Beeley, J. G., Bovell, D. L., Lu, J. R., Zhao, X., Cooper, A., and Kennedy, M. W. (2009) Latherin: a surfactant protein of horse sweat and saliva PLoS One 4, e5726 10.1371/journal.pone.0005726
28. Vance, S. J., McDonald, R. E., Cooper, A., Smith, B. O., and Kennedy, M. W. (2013) The structure of latherin, a surfactant allergen protein from horse sweat and saliva J. R. Soc., Interface 10, 20130453 10.1098/rsif.2013.0453
29. Tan, K. W., Jobichen, C., Ong, T. C., Gao, Y. F., Tiong, Y. S., Wong, K. N., Chew, F. T., Sivaraman, J., and Mok, Y. K. (2012) Crystal structure of Der f 7, a dust mite allergen from Dermatophagoides farinae PLoS One 7, e44850 10.1371/journal.pone.0044850
30. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260 10.1006/abio.2000.4880
31. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr., Sect. D: Biol. Crystallogr. 68, 352-367 10.1107/S0907444912001308
32. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132 10.1107/S0907444904019158
33. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. In Methods in Enzymology. Vol. 276: Macromolecular Crystallography, Part A (Carter, C. W., Jr. and Sweet, R. M., Eds.) pp 307-326, Academic Press, New York.
34. Fulcher, M. L. and Randell, S. H. (2012) Human nasal and tracheo-bronchial respiratory epithelial cell culture Methods Mol. Biol. 945, 109-121 10.1007/978-1-62703-125-7-8
35. Worthington, E. N. and Tarran, R. (2011) Methods for ASL measurements and mucus transport rates in cell cultures Methods Mol. Biol. 742, 77-92 10.1007/978-1-61779-120-8-5
36. Choi, H.-C., Kim, C. S. K., and Tarran, R. (2015) Automated acquisition and analysis of airway surface liquid height by confocal microscopy Am. J. Physiol. Lung Cell. Mol. Physiol. 309, L109-118 10.1152/ajplung.00027.2015
37. Suresh, G. K. and Soll, R. F. (2005) Overview of surfactant replacement trials J. Perinatol. 25 (Suppl. 2) S40-S44 10.1038/sj.jp.7211320
38. Gaillard, E. a., Kota, P., Gentzsch, M., Dokholyan, N. V., Stutts, M. J., and Tarran, R. (2010) Regulation of the epithelial Na+ channel and airway surface liquid volume by serine proteases Pfluegers Arch. 460, 1-17 10.1007/s00424-010-0827-z
39. Tsou, Y.-A., Chen, C.-M., Lin, T.-C., Hu, F.-W., Tai, C.-J., Chen, H.-C., Yeh, T.-H., Harn, H.-J., Tsai, M.-H., and Jan, C.-I. (2013) Decreased SPLUNC1 expression is associated with Pseudomonas infection in surgically treated chronic rhinosinusitis patients who may require repeated sinus surgery Laryngoscope 123, 845-851 10.1002/lary.23871
40. Romaniuk, J. A. H. and Cegelski, L. (2015) Bacterial cell wall composition and the influence of antibiotics by cell-wall and whole-cell NMR Philos. Trans. R. Soc., B 370, 20150024 10.1098/rstb.2015.0024