Linocin and OmpW are involved in attachment of the cystic fibrosis-associated pathogen Burkholderia cepacia complex to lung epithelial cells and protect mice against infection

Infection and Immunity

Volumn 84, Issue 5, 2016, Pages 1424-1437

  McClean, Siobhán ^a   Healy, Marc E ^b   Collins, Cassandra ^a   Carberry, Stephen ^b   O'Shaughnessy, Luke ^b   Dennehy, Ruth ^a   Adams, Áine ^b   Kennelly, Helen ^b   Corbett, Jennifer M ^b   Carty, Fiona ^b   Cahill, Laura A ^b   Callaghan, Máire ^a   English, Karen ^b   Mahon, Bernard P ^b   Doyle, Sean ^b   Shinoy, Minu ^a  

^a DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTIGEN; BACTERIAL PROTEIN; LINCOMYCIN; OMPW PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ADHESIN; BACTERIAL VACCINE; BACTERIOCIN; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS; CELL ADHESION; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE RESPONSE; EPITHELIUM CELL; ESCHERICHIA COLI; HOST CELL; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNIZATION; IN VIVO STUDY; LUNG ALVEOLUS CELL; LUNG INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; ANIMAL; BACTERIUM ADHERENCE; BAGG ALBINO MOUSE; BURKHOLDERIA INFECTIONS; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BACTERIOCINS; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; HUMANS; MICE, INBRED BALB C; RECOMBINANT PROTEINS; TREATMENT OUTCOME;

EID: 84964545128     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01248-15     Document Type: Article

References (65)

1. Mishra RP, Oviedo-Orta E, Prachi P, Rappuoli R, Bagnoli F. 2012. Vaccines and antibiotic resistance. Curr Opin Microbiol 15:596-602. http://dx.doi.org/10.1016/j.mib.2012.08.002.
2. Masignani V, Rappuoli R, Pizza M. 2002. Reverse vaccinology: a genome-based approach for vaccine development. Expert Opin Biol Ther 2:895-905. http://dx.doi.org/10.1517/14712598.2.8.895.
3. Pizza M, Scarlato V, Masignani V, Giuliani MM, Arico B, Comanducci M, Jennings GT, Baldi L, Bartolini E, Capecchi B, Galeotti CL, Luzzi E, Manetti R, Marchetti E, Mora M, Nuti S, Ratti G, Santini L, Savino S, Scarselli M, Storni E, Zuo P, Broeker M, Hundt E, Knapp B, Blair E, Mason T, Tettelin H, Hood DW, Jeffries AC, Saunders NJ, Granoff DM, Venter JC, Moxon ER, Grandi G, Rappuoli R. 2000. Identification of vaccine candidates against serogroup B meningococcus by wholegenome sequencing. Science 287:1816-1820. http://dx.doi.org/10.1126/science.287.5459.1816.
4. Felgner PL, Kayala MA, Vigil A, Burk C, Nakajima-Sasaki R, Pablo J, Molina DM, Hirst S, Chew JS, Wang D, Tan G, Duffield M, Yang R, Neel J, Chantratita N, Bancroft G, Lertmemongkolchai G, Davies DH, Baldi P, Peacock S, Titball RW. 2009. A Burkholderia pseudomallei protein microarray reveals serodiagnostic and cross-reactive antigens. Proc Natl Acad Sci U S A 106:13499-13504. http://dx.doi.org/10.1073/pnas.0812080106.
5. Dennehy R, McClean S. 2012. Immunoproteomics: the key to discovery of new vaccine antigens against bacterial respiratory infections. Curr Protein Pept Sci 13:807-815. http://dx.doi.org/10.2174/138920312804871184.
6. Altindis E, Tefon BE, Yildirim V, Ozcengiz E, Becher D, Hecker M, Ozcengiz G. 2009. Immunoproteomic analysis of Bordetella pertussis and identification of new immunogenic proteins. Vaccine 27:542-548. http://dx.doi.org/10.1016/j.vaccine.2008.11.020.
7. Tefon BE, Maass S, Ozcengiz E, Becher D, Hecker M, Ozcengiz G. 2011. A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins. Vaccine 29:3583-3595. http://dx.doi.org/10.1016/j.vaccine.2011.02.086.
8. Coenye T, Vandamme P, Govan JR, LiPuma JJ. 2001. Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39: 3427-3436. http://dx.doi.org/10.1128/JCM.39.10.3427-3436.2001.
9. Coenye T, Vandamme P, LiPuma JJ, Govan JR, Mahenthiralingam E. 2003. Updated version of the Burkholderia cepacia complex experimental strain panel. J Clin Microbiol 41:2797-2798. http://dx.doi.org/10.1128/JCM.41.6.2797-2798.2003.
10. Mahenthiralingam E, Baldwin A, Drevinek P, Vanlaere E, Vandamme P, Lipuma JJ, Dowson CG. 2006. Multilocus sequence typing breathes life into a microbial metagenome. PLoS One 1:e17. http://dx.doi.org/10.1371/journal.pone.0000017.
11. Peeters C, Zlosnik JE, Spilker T, Hird TJ, LiPuma JJ, Vandamme P. 2013. Burkholderia pseudomultivorans sp. nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst Appl Microbiol 36:483-489. http://dx.doi.org/10.1016/j.syapm.2013.06.003.
12. McClean S, Callaghan M. 2009. Burkholderia cepacia complex: epithelial cell-pathogen confrontations and potential for therapeutic intervention. J Med Microbiol 58:1-12. http://dx.doi.org/10.1099/jmm.0.47788-0.
13. Drevinek P, Mahenthiralingam E. 2010. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 16:821-830. http://dx.doi.org/10.1111/j.1469-0691.2010.03237.x.
14. Courtney JM, Dunbar KE, McDowell A, Moore JE, Warke TJ, Stevenson M, Elborn JS. 2004. Clinical outcome of Burkholderia cepacia complex infection in cystic fibrosis adults. J Cyst Fibros 3:93-98. http://dx.doi.org/10.1016/j.jcf.2004.01.005.
15. Callaghan M, McClean S. 2012. Bacterial host interactions in cystic fibrosis. Curr Opin Microbiol 15:71-77. http://dx.doi.org/10.1016/j.mib.2011.11.001.
16. Chernish RN, Aaron SD. 2003. Approach to resistant gram-negative bacterial pulmonary infections in patients with cystic fibrosis. Curr Opin Pulm Med 9:509-515. http://dx.doi.org/10.1097/00063198-200311000-00011.
17. Saiman L, Tabibi S, Starner TD, San Gabriel P, Winokur PL, Jia HP, McCray PB, Jr, Tack BF. 2001. Cathelicidin peptides inhibit multiply antibiotic-resistant pathogens from patients with cystic fibrosis. Antimicrob Agents Chemother 45:2838-2844. http://dx.doi.org/10.1128/AAC.45.10.2838-2844.2001.
18. Baird RM, Brown H, Smith AW, Watson ML. 1999. Burkholderia cepacia is resistant to the antimicrobial activity of airway epithelial cells. Immunopharmacology 44:267-272. http://dx.doi.org/10.1016/S0162-3109(99)00122-8.
19. McDowell A, Mahenthiralingam E, Dunbar KE, Moore JE, Crowe M, Elborn JS. 2004. Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation. J Med Microbiol 53:663-668. http://dx.doi.org/10.1099/jmm.0.45557-0.
20. Baldwin A, Mahenthiralingam E, Drevinek P, Pope C, Waine DJ, Henry DA, Speert DP, Carter P, Vandamme P, Lipuma JJ, Dowson CG. 2008. Elucidating global epidemiology of Burkholderia multivorans in cases of cystic fibrosis by multilocus sequence typing. J Clin Microbiol 46:290-295. http://dx.doi.org/10.1128/JCM.01818-07.
21. Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE, Av-Gay Y, Vandamme P. 2000. DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. J Clin Microbiol 38:3165-3173.
22. Mahenthiralingam E, Baldwin A, Dowson CG. 2008. Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539-1551. http://dx.doi.org/10.1111/j.1365-2672.2007.03706.x.
23. Vardi A, Sirigou A, Lalayanni C, Kachrimanidou M, Kaloyannidis P, Saloum R, Anagnostopoulos A, Sotiropoulos D. 4 October 2012. An outbreak of Burkholderia cepacia bacteremia in hospitalized hematology patients selectively affecting those with acute myeloid leukemia. Am J Infect Control http://dx.doi.org/10.1016/j.ajic.2012.04.325.
24. Fishman JA. 2011. Infections in immunocompromised hosts and organ transplant recipients: essentials. Liver Transpl 17(Suppl 3):S34-S37. http://dx.doi.org/10.1002/lt.22378.
25. Bertot GM, Restelli MA, Galanternik L, Aranibar Urey RC, Valvano MA, Grinstein S. 2007. Nasal immunization with Burkholderia multivorans outer membrane proteins and the mucosal adjuvant adamantylamide dipeptide confers efficient protection against experimental lung infections with B. multivorans and B. cenocepacia. Infect Immun 75:2740-2752. http://dx.doi.org/10.1128/IAI.01668-06.
26. Makidon PE, Knowlton J, Groom JV, II, Blanco LP, LiPuma JJ, Bielinska AU, Baker JR, Jr. 2010. Induction of immune response to the 17 kDa OMPABurkholderia cenocepacia polypeptide and protection against pulmonary infection in mice after nasal vaccination with anOMPnanoemulsion-based vaccine. Med Microbiol Immunol 199:81-92. http://dx.doi.org/10.1007/s00430-009-0137-2.
27. Caraher E, Duff C, Mullen T, Mc Keon S, Murphy P, Callaghan M, McClean S. 2007. Invasion and biofilm formation of Burkholderia dolosa is comparable with Burkholderia cenocepacia and Burkholderia multivorans. J Cyst Fibros 6:49-56. http://dx.doi.org/10.1016/j.jcf.2006.05.007.
28. Liu DF, Phillips E, Wizemann TM, Siegel MM, Tabei K, Cowell JL, Tuomanen E. 1997. Characterization of a recombinant fragment that contains a carbohydrate recognition domain of the filamentous hemagglutinin. Infect Immun 65:3465-3468.
29. Marzouqi I, Richmond P, Fry S, Wetherall J, Mukkur T. 2010. Development of improved vaccines against whooping cough: current status. Hum Vaccin 6:543-553. http://dx.doi.org/10.4161/hv.6.7.11413.
30. Sajjan U, Wu Y, Kent G, Forstner J. 2000. Preferential adherence of cable-piliated Burkholderia cepacia to respiratory epithelia of CF knockout mice and human cystic fibrosis lung explants. J Med Microbiol 49: 875-885. http://dx.doi.org/10.1099/0022-1317-49-10-875.
31. Mil-Homens D, Leca MI, Fernandes F, Pinto SN, Fialho AM. 2014. Characterization of BCAM0224, a multifunctional trimeric autotransporter from the human pathogen Burkholderia cenocepacia. J Bacteriol 196:1968-1979. http://dx.doi.org/10.1128/JB.00061-14.
32. Mil-Homens D, Fialho AM. 2012. A BCAM0223 mutant of Burkholderia cenocepacia is deficient in hemagglutination, serum resistance, adhesion to epithelial cells and virulence. PLoS One 7:e41747. http://dx.doi.org/10.1371/journal.pone.0041747.
33. Henry DA, Campbell ME, LiPuma JJ, Speert DP. 1997. Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35:614-619.
34. Goncz KK, Feeney L, Gruenert DC. 1999. Differential sensitivity of normal and cystic fibrosis airway epithelial cells to epinephrine. Br J Pharmacol 128:227-233. http://dx.doi.org/10.1038/sj.bjp.0702772.
35. Sylvester FA, Sajjan US, Forstner JF. 1996. Burkholderia (basonym Pseudomonas) cepacia binding to lipid receptors. Infect Immun 64:1420-1425.
36. Shinoy M, Dennehy R, Coleman L, Carberry S, Schaffer K, Callaghan M, Doyle S, McClean S. 2013. Immunoproteomic analysis of proteins expressed by two related pathogens, Burkholderia multivorans and Burkholderia cenocepacia, during human infection. PLoS One 8:e80796. http://dx.doi.org/10.1371/journal.pone.0080796.
37. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
38. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Biochemistry 76:4350-4354.
39. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2007. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856-2860. http://dx.doi.org/10.1038/nprot.2006.468.
40. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
41. UniProt Consortium. 2014. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 42:D191-D198. http://dx.doi.org/10.1093/nar/gkt1140.
42. Winsor GL, Khaira B, Van Rossum T, Lo R, Whiteside MD, Brinkman FS. 2008. The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24:2803-2804. http://dx.doi.org/10.1093/bioinformatics/btn524.
43. Valdes-Stauber N, Scherer S. 1994. Isolation and characterization of linocin M18, a bacteriocin produced by Brevibacterium linens. Appl Environ Microbiol 60:3809-3814.
44. Rosenkrands I, Rasmussen PB, Carnio M, Jacobsen S, Theisen M, Andersen P. 1998. Identification and characterization of a 29-kilodalton protein from Mycobacterium tuberculosis culture filtrate recognized by mouse memory effector cells. Infect Immun 66:2728-2735.
45. Sutter M, Boehringer D, Gutmann S, Gunther S, Prangishvili D, Loessner MJ, Stetter KO, Weber-Ban E, Ban N. 2008. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15:939-947. http://dx.doi.org/10.1038/nsmb.1473.
46. McPhee JB, Tamber S, Bains M, Maier E, Gellatly S, Lo A, Benz R, Hancock RE. 2009. The major outer membrane protein OprG of Pseudomonas aeruginosa contributes to cytotoxicity and forms an anaerobically regulated, cation-selective channel. FEMS Microbiol Lett 296:241-247. http://dx.doi.org/10.1111/j.1574-6968.2009.01651.x.
47. Harmer C, Alnassafi K, Hu H, Elkins M, Bye P, Rose B, Cordwell S, Triccas JA, Harbour C, Manos J. 2013. Modulation of gene expression by Pseudomonas aeruginosa during chronic infection in the adult cystic fibrosis lung. Microbiology 159:2354-2363. http://dx.doi.org/10.1099/mic.0.066985-0.
48. Nandi B, Nandy RK, Sarkar A, Ghose AC. 2005. Structural features, properties and regulation of the outer-membrane proteinW(OmpW) of Vibrio cholerae. Microbiology 151:2975-2986. http://dx.doi.org/10.1099/mic.0.27995-0.
49. McClean S. 2012. Eight stranded beta-barrel and related outer membrane proteins: role in bacterial pathogenesis. Protein Pept Lett 19:1013-1025. http://dx.doi.org/10.2174/092986612802762688.
50. Qian R, Chu W, Mao Z, Zhang C, Wei Y, Yu L. 2007. Expression, characterization and immunogenicity of a major outer membrane protein from Vibrio alginolyticus. Acta Biochim Biophys Sin (Shanghai) 39:194-200. http://dx.doi.org/10.1111/j.1745-7270.2007.00268.x.
51. Wei B, Dalwadi H, Gordon LK, Landers C, Bruckner D, Targan SR, Braun J. 2001. Molecular cloning of a Bacteroides caccae TonB-linked outer membrane protein identified by an inflammatory bowel disease marker antibody. Infect Immun 69:6044-6054. http://dx.doi.org/10.1128/IAI.69.10.6044-6054.2001.
52. Singh R, Shasany AK, Aggarwal A, Sinha S, Sisodia BS, Khanuja SP, Misra R. 2007. Low molecular weight proteins of outer membrane of Salmonella Typhimurium are immunogenic in Salmonella induced reactive arthritis revealed by proteomics. Clin Exp Immunol 148:486-493. http://dx.doi.org/10.1111/j.1365-2249.2007.03362.x.
53. Maiti B, Shetty M, Shekar M, Karunasagar I, Karunasagar I. 2012. Evaluation of two outer membrane proteins, Aha1 and OmpW of Aeromonas hydrophila as vaccine candidate for common carp. Vet Immunol Immunopathol 149:298-301. http://dx.doi.org/10.1016/j.vetimm.2012.07.013.
54. Riedel K, Carranza P, Gehrig P, Potthast F, Eberl L. 2006. Towards the proteome of Burkholderia cenocepacia H111: setting up a 2-DE reference map. Proteomics 6:207-216. http://dx.doi.org/10.1002/pmic.200500097.
55. Nieves W, Heang J, Asakrah S, Honerzu Bentrup K, Roy CJ, Morici LA. 2010. Immunospecific responses to bacterial elongation factor Tu during Burkholderia infection and immunization. PLoS One 5:e14361. http://dx.doi.org/10.1371/journal.pone.0014361.
56. Bevivino A, Pirone L, Pilkington R, Cifani N, Dalmastri C, Callaghan M, Ascenzioni F, McClean S. 2012. Interaction of environmental Burkholderia cenocepacia strains with cystic fibrosis and non-cystic fibrosis bronchial epithelial cells in vitro. Microbiology 158:1325-1333. http://dx.doi.org/10.1099/mic.0.056986-0.
57. Chiu CH, Ostry A, Speert DP. 2001. Invasion of murine respiratory epithelial cells in vivo by Burkholderia cepacia. J Med Microbiol 50:594-601. http://dx.doi.org/10.1099/0022-1317-50-7-594.
58. Duff C, Murphy PG, Callaghan M, McClean S. 2006. Differences in invasion and translocation of Burkholderia cepacia complex species in polarised lung epithelial cells in vitro. Microb Pathog 41:183-192. http://dx.doi.org/10.1016/j.micpath.2006.07.005.
59. Sajjan U, Moreira J, Liu M, Humar A, Chaparro C, Forstner J, Keshavjee S. 2004. A novel model to study bacterial adherence to the transplanted airway: inhibition of Burkholderia cepacia adherence to human airway by dextran and xylitol. J Heart Lung Transplant 23:1382-1391. http://dx.doi.org/10.1016/j.healun.2003.09.023.
60. Schwab U, Leigh M, Ribeiro C, Yankaskas J, Burns K, Gilligan P, Sokol P, Boucher R. 2002. Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun 70:4547-4555. http://dx.doi.org/10.1128/IAI.70.8.4547-4555.2002.
61. Wu W, Huang J, Duan B, Traficante DC, Hong H, Risech M, Lory S, Priebe GP. 2012. Th17-stimulating protein vaccines confer protection against Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 186:420-427. http://dx.doi.org/10.1164/rccm.201202-0182OC.
62. Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JR, Taylor P, Vandamme P. 2000. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38:910-913.
63. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS. 2010. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608-1615. http://dx.doi.org/10.1093/bioinformatics/btq249.
64. Pappin DJ, Hojrup P, Bleasby AJ. 1993. Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 3:327-332. http://dx.doi.org/10.1016/0960-9822(93)90195-T.
65. European Parliament and the Council of the European Union. 2010. Directive 2010/63/Eu on the protection of animals used for scientific purposes, p b7. Institute for Health and Consumer Protection, Ispra, Italy.