Evidence and Role for Bacterial Mucin Degradation in Cystic Fibrosis Airway Disease

PLoS Pathogens

Volumn 12, Issue 8, 2016, Pages

  Flynn, Jeffrey M ^a   Niccum, David ^a   Dunitz, Jordan M ^a   Hunter, Ryan C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MUCIN; RNA 16S; SHORT CHAIN FATTY ACID; BACTERIAL RNA; PROPIONIC ACID DERIVATIVE;

ARTICLE; BACTERIAL GROWTH; CARBON SOURCE; CLINICAL ARTICLE; CYSTIC FIBROSIS; CYSTIC FIBROSIS AIRWAY DISEASE; DNA EXTRACTION; FUSOBACTERIUM NUCLEATUM; GENE DELETION; GENE EXPRESSION; GENE SEQUENCE; HUMAN; INFLAMMATION; LUNG INFECTION; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; NONHUMAN; PHENOTYPE; PREVOTELLA MELANINOGENICA; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPUTUM ANALYSIS; STAPHYLOCOCCUS; STREPTOCOCCUS PARASANGUINIS; FEMALE; GENETICS; LUNG; MALE; METABOLISM; MICROBIOLOGY;

CYSTIC FIBROSIS; FEMALE; HUMANS; LUNG; MALE; MUCINS; PROPIONATES; PSEUDOMONAS AERUGINOSA; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

EID: 84984856617     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005846     Document Type: Article

References (63)

1. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science1989; 245:1066–1073. 2475911
2. Gibson RL, Burns JL, Ramsey BW, Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med. 2003; 168:918–951. 14555458
3. Carmody LA, Zhao J, Schloss PD, Petrosino JF, Murray S, Young VB, et al. Changes in cystic fibrosis airways microbiota at pulmonary exacerbation. Ann Am Thorac Soc. 2013; 10:179–187. doi: 10.1513/AnnalsATS.201211-107OC23802813
4. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Kehagia V, et al. Use of 16S rRNA gene profiling by terminal restriction fragment length polymorphism analysis to compare bacterial communities in sputum and mouthwash samples from patients with cystic fibrosis. J Clin Microbiol. 2006; 44:2601–2604. 16825392
5. Zemanick ET, Wagner BD, Robertson CE, Stevens MJ, Szefler SJ, Accurso FJ, et al. Assessment of airway microbiota and inflammation in cystic fibrosis using multiple sampling methods. Ann Am Thorac Soc. 2015; 12:221–229. doi: 10.1513/AnnalsATS.201407-310OC25474078
6. Hunter RC, Klepac-Ceraj V, Lorenzi MM, Grotzinger H, Martin TR, Newman DK, Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am J Respir Cell Mol Biol. 2012; 47:738–745. doi: 10.1165/rcmb.2012-0088OC22865623
7. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI, Host-bacterial mutualism in the human intestine. Science2005; 307:1915–1920. 15790844
8. Cole AM, Dewan P, Ganz T, Innate antimicrobial activity of nasal secretions. Infect Immun. 1999; 67:3267–3275. 10377100
9. Fahy JV, Dickey BF, Airway mucus function and dysfunction. New Engl J Med. 2010; 363:2233–2247. doi: 10.1056/NEJMra091006121121836
10. Rayner RJ, Wiseman M, Cordon SM, Norman D, Hiller EJ, Shale DJ, Inflammatory markers in cystic fibrosis. Resp Med. 1991; 85:139–145.
11. Konstan MW, Hilliard KA, Norvell TM, Berger M, Bronchoalveolar lavage findings in cystic fibrosis patients with stable, clinically mild lung disease suggest ongoing infection and inflammation. Am J Resp Crit Care Med. 1994; 150:448–454. 8049828
12. Bonfield TL, Panuska JR, Konstan MW, Hilliard JB, Ghnaim H, Berger M, Inflammatory cytokines in cystic fibrosis lungs. Am J Resp Crit Care Med. 1995; 152:2111–2118. 8520783
13. Soong LB, Ganz T, Ellison A, Caughey GH, Purification and characterization of defensins from cystic fibrosis sputum. Inflamm Res. 1997; 46:98–102. 9098722
14. Ghorbani P, Santhakumar P, Hu Q, Djiadeu P, Wolever TM, Palaniyar N, et al. Short chain fatty acids affect cystic fibrosis airway inflammation and bacterial growth. Eur Respir J. 2015; ERJ-01436.
15. Palmer KL, Mashburn LM, Singh PK, Whiteley M, Cystic fibrosis sputum supports growth and cues key aspects of P. aeruginosa physiology. J Bacteriol. 2005; 187:5267–5277. 16030221
16. LaBauve AE, Wargo MJ, Detection of host-derived sphingosine by Pseudomonas aeruginosa is important for survival in the murine lung. PLoS Pathogens. 2014; e1003889. doi: 10.1371/journal.ppat.100388924465209
17. Son MS, Matthews WJ, Jr.Kang Y, Nguyen D, Hoang TT, In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun. 2007. 75:5313–5324. 17724070
18. Henderson AG, Ehre C, Button B, Abdullah LH, Cai LH, Leigh MW, et al. Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J Clin Invest. 2014; 124:3047–3060. doi: 10.1172/JCI7346924892808
19. Kreda SM, Davis CW, Rose MC, CFTR, mucins, and mucus obstructions in cystic fibrosis. Cold Spring Harbor perspectives in medicine. 2012; 2.9:a009589.
20. Roberton AM, McKenzie CG, Sharfe N, Stubbs LB, A glycosulphatase that removes sulphate from mucus glycoprotein. Biochem J. 1993; 293:683–689. 8352735
21. Wickstrom C, Herzberg MC, Beighton D, Svensäter G, Proteolytic degradation of human salivary MUC5B by dental biofilms. Microbiol. 2009; 155:2866–2872.
22. Durrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM, The mucin degrader Akkermansia muciniphilia is an abundant resident of the human intestinal tract. Appl Environ Microbiol2007; 74:1646–1648. 18083887
23. Bradshaw DJ, Homer KA, Marsh PD, Beighton D, Metabolic cooperation in oral microbial communities during growth on mucin. Microbiology. 1994; 140:3407–3412. 7881558
24. Kolenbrander P, Multispecies communities: interspecies interactions influence growth on saliva as sole nutritional source. Int J Oral Sci. 2011; 3:49–54. doi: 10.4248/IJOS1102521485308
25. Cameron EA, Sperandio V, Frenemies: Signaling and nutritional integration in pathogen-microbiota-host interactions. Cell Host & Microbe. 2015; 18:275–284.
26. Schwab U, Abdullah LH, Perimutt OS, Albert D, Davis CW, Arnold RR, Yankaskas JR, Gilligan P, Neubauer H, Randell SH, Boucher RC, Localization of Burkholderia cepecia complex in cystic fibrosis lungs and interaction with Pseudomonas aeruginosa in hypoxic mucus. Infect Immun. 2014; 82:4729–4745. doi: 10.1128/IAI.01876-1425156735
27. Field TR, Sibley CD, Parkins MD, Rabin HR, Surette MG, The genus Prevotella in cystic fibrosis airways. Anaerobe. 2010; 16:337–344. doi: 10.1016/j.anaerobe.2010.04.00220412865
28. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, Muhlebach MS, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Resp Crit Care Med. 2008; 177:995–1001. doi: 10.1164/rccm.200708-1151OC18263800
29. Mirkovic B, Murray MA, Lavella GM, Molloy K, Azim AA, Gunaratnam C, et al. The role of short-chain fatty acids, produced by anaerobic bacteria, in the cystic fibrosis airway. Am J Resp Crit Care Med. 2015; 192:1314–1324. doi: 10.1164/rccm.201505-0943OC26266556
30. Roberton AM, Corfield AP, Tannock GW, Mucin degradation and its significance in inflammatory conditions of the gastrointestinal tract. In: Medical importance of the normal microflora. Springer; 1999. pp. 222–252.
31. Barth AL, Pitt TL, The high amino acid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa. J Med Microbiol. 1996; 45:110–119. 8683546
32. Willner D, Haynes MR, Furlan M, Schmeider R, Lim YW, Rainey PB, et al. Spatial distribution of microbial communities in the cystic fibrosis lung. ISME J. 2012; 6:471–474. doi: 10.1038/ismej.2011.10421796216
33. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM, et al. The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS One2012; 7:e45001. doi: 10.1371/journal.pone.004500123049765
34. Blainey PR, Milla CE, Cornfield DN, Quake SR, Quantitative analysis of the human airway microbial ecology reveals a pervasive signature for cystic fibrosis. Sci Transl Med. 2012; 4:153ra130. 23019655
35. Wright DP, Rosendale DI, Roberton AM, Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucins. FEMS Microbiol Lett. 2000; 190:73–79. 10981693
36. Garrity G, Brenner DJ, Krieg NR, Stanley JR, Bergey’s Manual of Systematic Bacteriology. Vol 2: the proteobacteria, Part B: the gammaproteobacteria. Springer; 2005. pp. 364.
37. Staudinger BJ, Muller JF, Halldorsson S, Boles B, Angermeyer A, Nguyen D, et al. Conditions associated with the cystic fibrosis defect promote chronic Pseudomonas aeruginosa infection. Am J Resp Crit Care Med. 2014; 189:812–824. doi: 10.1164/rccm.201312-2142OC24467627
38. Niederman R, Buyle-Bodin Y, Lu BY, Robinson P, Naleway C, Short-chain carboxylic acid concentration in human gingical crevicular fluid. J Dental Res. 1997; 76:575–579.
39. Henke MO, John G, Rheineck C, Chillappagari S, Naehrlich L, Rubin BK, Serine proteases degrade airway mucins in cystic fibrosis. Infect Immun. 2011; 79:3438–3444. doi: 10.1128/IAI.01252-1021646446
40. Korgaonkar AK, Whiteley M, Pseudomonas aeruginosa enhances production of antimicrobial in response to N-acetylglucosamine and peptidoglycan. J Bacteriol. 2011; 193:909–917. doi: 10.1128/JB.01175-1021169497
41. Aristoteli L, Wilcox MDP, Mucin degradation mechanisms by distinct Pseudomonas aeruginosa isolates. Infect Immun. 2003; 71:5565–5575. 14500475
42. Robinson CV, Elkins MR, Bialkowski KM, Thornton DJ, Kertesz MA, Desulfurization of mucin by Pseudomonas aeruginosa: influence of sulfate in the lungs of cystic fibrosis patients. J Med Microbiol. 2012; 61:1644–1653. doi: 10.1099/jmm.0.047167-022918866
43. Høverstad T, Midtvedt T, Short-chain fatty acids in germfree mice and rats. J Nutr. 1986; 116:1772–1776. 3761032
44. Dowling RB, Johnson M, Cole PJ, Wilson R, Effect of fluticasone propionate and salmetrol on Pseudomonas aeruginosa infection of the respiratory mucosa in vitro. Eur Resp J. 1999; 14:363–369.
45. Hampton TH, Green DM, Cutting GR, Morrison HG, Sogin ML, Gifford AH, et al. The microbiome in pediatric cystic fibrosis patients: the role of shared environment suggests a window of intervention. Microbiome. 2014; 2:14. doi: 10.1186/2049-2618-2-1425071935
46. Madan JC, Koestler DC, Stanton BA, Davidson L, Moulton LA, Housman ML, et al. Serial analysis of the gut and respiratory microbiome in cystic fibrosis in infancy: Interaction between intestinal and respiratory tracts and impact of nutritional exposures. mBio. 2012; 3:e00251–12.
47. Ramsey BW, Pepe MS, Quan JM, Otto KL, Montgomery AB, Williams-Warren J, et al. Intermittent administration of inhaled tobramycin in patients with cystic fibrosis. N Engl J Med. 1999; 340:23–30. 9878641
48. Saiman L, Anstead M, Mayer-Hamblett N, Lands LC, Kloster M, Hocevar-Trnka J, et al. Effect of azithromycin on pulmonary function in patients with cystic fibrosis uninfected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2010; 303:1707–15. doi: 10.1001/jama.2010.56320442386
49. Hurley MN, Ariff AA, Bertenshaw C, Bhatt J, Smyth AR, Results of antibiotic susceptibility testing do not influence clinical outcome in children with cystic fibrosis. J Cyst Fibros. 2012; 11:288–92. doi: 10.1016/j.jcf.2012.02.00622436723
50. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, Knapp AA, et al. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics, and Pseudomonas aeruginosa. Environ Microbiol. 2010; 12:1293–1303. doi: 10.1111/j.1462-2920.2010.02173.x20192960
51. Jorth P, Staudinger BJ, Wu X, Hisert KB, Garudathri J, Harding CL, et al. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microb. 2015; 18:307–319.
52. McDonald DM, Angiogenesis and remodeling of airway vasculature in chronic inflammation. Am J Respir Crit Care Med. 2001; 164:39–45.
53. Badalamenti J, Hunter RC, Complete genome sequence of Achromobacter xylosoxidans MN001, a cystic fibrosis airway isolate. Genome Announc. 2015; 3:e00947–15. doi: 10.1128/genomeA.00947-1526294635
54. Marsili E, Rollefson JB, Baron DB, Hozalski RM, Bond DR, Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms. Appl Environ Microbiol. 2008; 74:7329–37. doi: 10.1128/AEM.00177-0818849456
55. Wickstrom C, Svensäter Salivary gel-forming mucin MUC5B –a nutrient for dental plaque bacteria. Oral Microbiol Immunol. 2008; 23:177–182. doi: 10.1111/j.1399-302X.2007.00407.x18402602
56. Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A, Becker A, et al. Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotech. 2016. In press. doi: 10.1038/nbt.3601
57. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7:335–336. doi: 10.1038/nmeth.f.30320383131
58. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD, PANDAseq: paired-end assembler for Illumina sequences. BMC Bioinformatics. 2012; 13:31. doi: 10.1186/1471-2105-13-3122333067
59. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72:5069–5072. 16820507
60. White JR, Nagarajan N, Pop M, Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol. 2009; 5: e1000352. doi: 10.1371/journal.pcbi.100035219360128
61. Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK, 2003. The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species stain ANA-3. Appl Environ Microbiol. 69:2800–2809. 12732551
62. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, Smith HO, Enzymatic assembly of DNA molecules up to several hundred kilobases. Nature Methods2009; 6:343–345. doi: 10.1038/nmeth.131819363495
63. Hunter RC, Asfour F, Dingemans J, Osuna B, Samad T, Malfroot et al. Ferrous iron is a significant component of bioavailable iron in the cystic fibrosis airways. mBio. 2013; 4:e00557–13.