The role of short-chain fatty acids, produced by anaerobic bacteria, in the cystic fibrosis airway

American Journal of Respiratory and Critical Care Medicine

Volumn 192, Issue 11, 2015, Pages 1314-1324

  Mirković, Bojana ^a   Murray, Michelle A ^a   Lavelle, Gillian M ^a   Molloy, Kevin ^a   Azim, Ahmed Abdul ^a   Gunaratnam, Cedric ^a   Healy, Fiona ^b   Slattery, Dubhfeasa ^b   McNally, Paul ^c   Hatch, Joe ^d   Wolfgang, Matthew ^d   Tunney, Michael M ^e   Muhlebach, Marianne S ^d   Devery, Rosaleen ^f   Greene, Catherine M ^a   McElvaney, Noel G ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b CHILDREN S UNIVERSITY HOSPITAL   (Ireland)

^c OUR LADY S CHILDREN S HOSPITAL   (Ireland)

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

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^f DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

Anaerobic bacteria; Cystic fibrosis; Inflammation; Short chain fatty acids

Indexed keywords

ACETIC ACID DERIVATIVE; BUTYRIC ACID DERIVATIVE; INTERLEUKIN 8; MESSENGER RNA; PERTUSSIS TOXIN; PROPIONIC ACID DERIVATIVE; RNA 16S; SHORT CHAIN FATTY ACID; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FATTY ACID;

ACTINOMYCES; ACTINOMYCES ODONTOLYTICUS; ADOLESCENT; ADULT; ANAEROBIC BACTERIUM; ARTICLE; BACTERIUM CULTURE; BRONCHUS MUCOSA; CHILD; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY ACID BLOOD LEVEL; FEMALE; FUSOBACTERIUM NUCLEATUM; GAS CHROMATOGRAPHY; HUMAN; INFANT; INVESTIGATIVE PROCEDURES; LASER SCANNING CYTOMETRY; LUNG LAVAGE; MAJOR CLINICAL STUDY; MALE; PREVALENCE; PREVOTELLA MELANINOGENICA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; STREPTOCOCCUS SANGUINIS; SUPERNATANT; VEILLONELLA PARVULA; WESTERN BLOTTING; AGE; BIOSYNTHESIS; BRONCHOALVEOLAR LAVAGE FLUID; EPITHELIUM CELL; MICROBIOLOGY; MIDDLE AGED; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; RESPIRATORY MUCOSA; UPREGULATION; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; BACTERIA, ANAEROBIC; BLOTTING, WESTERN; BRONCHOALVEOLAR LAVAGE FLUID; CHILD; CHILD, PRESCHOOL; CHROMATOGRAPHY, GAS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FATTY ACIDS; FEMALE; HUMANS; INFANT; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; RESPIRATORY MUCOSA; UP-REGULATION; YOUNG ADULT;

EID: 84949032357     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201505-0943OC     Document Type: Article

References (46)

1. Davies JC, Alton EWFW, Bush A. Cystic fibrosis. BMJ 2007;335:1255-1259.
2. Cohen TS, Prince A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat Med 2012;18:509-519.
3. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Høiby N, Molin S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 2012;10:841-851.
4. Bittar F, Richet H, Dubus JC, Reynaud-Gaubert M, Stremler N, Sarles J, Raoult D, Rolain JM. Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS One 2008;3: e2908.
5. Sibley CD, Grinwis ME, Field TR, Eshaghurshan CS, Faria MM, Dowd SE, Parkins MD, Rabin HR, Surette MG. Culture enriched molecular profiling of the cystic fibrosis airway microbiome. PLoS One 2011;6: e22702.
6. Hauser PM, Bernard T, Greub G, Jaton K, Pagni M, Hafen GM. Microbiota present in cystic fibrosis lungs as revealed by whole genome sequencing. PLoS One 2014;9: e90934.
7. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, Muhlebach MS, Wolfgang MC, Boucher R, Gilpin DF, McDowell A, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med 2008;177: 995-1001.
8. Worlitzsch D, Rintelen C, Böhm K, Wollschläger B, Merkel N, Borneff-Lipp M, Döring G. Antibiotic-resistant obligate anaerobes during exacerbations of cystic fibrosis patients. Clin Microbiol Infect 2009;15:454-460.
9. Delhaes L, Monchy S, Fréalle E, Hubans C, Salleron J, Leroy S, Prevotat A, Wallet F, Wallaert B, Dei-Cas E, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community-implications for therapeutic management. PLoS One 2012;7: e36313.
10. Zemanick ET, Harris JK, Wagner BD, Robertson CE, Sagel SD, Stevens MJ, Accurso FJ, Laguna TA. Inflammation and airway microbiota during cystic fibrosis pulmonary exacerbations. PLoS One 2013;8: e62917.
11. Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Karaoz U, Andersen GL, Brown R, Fujimura KE, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 2010;5: e11044.
12. Ulrich M, Beer I, Braitmaier P, Dierkes M, Kummer F, Krismer B, Schumacher U, Gräpler-Mainka U, Riethmüller J, Jensen PØ, et al. Relative contribution of Prevotella intermedia and Pseudomonas aeruginosa to lung pathology in airways of patients with cystic fibrosis. Thorax 2010;65:978-984.
13. Sibley CD, Duan K, Fischer C, Parkins MD, Storey DG, Rabin HR, Surette MG. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 2008;4: e1000184.
14. Pan Y, Teng D, Burke AC, Haase EM, Scannapieco FA. Oral bacteria modulate invasion and induction of apoptosis in HEp-2 cells by Pseudomonas aeruginosa. Microb Pathog 2009;46: 73-79.
15. Pustelny C, Komor U, Pawar V, Lorenz A, Bielecka A, Moter A, Gocht B, Eckweiler D, Müsken M, Grothe C, et al. Contribution of Veillonella parvula to Pseudomonas aeruginosa-mediated pathogenicity in a murine tumor model system. Infect Immun 2015; 83:417-429.
16. Field TR, Sibley CD, Parkins MD, Rabin HR, Surette MG. The genus Prevotella in cystic fibrosis airways. Anaerobe 2010;16: 337-344.
17. Duan K, Dammel C, Stein J, Rabin H, Surette MG. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 2003;50: 1477-1491.
18. Vinolo MAR, Rodrigues HG, Nachbar RT, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients 2011;3:858-876.
19. Wu J, Zhou Z, Hu Y, Dong S. Butyrate-induced GPR41 activation inhibits histone acetylation and cell growth. J Genet Genomics 2012; 39:375-384.
20. Xiong Y, Miyamoto N, Shibata K, Valasek MA, Motoike T, Kedzierski RM, Yanagisawa M. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci USA 2004;101:1045-1050.
21. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012;61:364-371.
22. Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, Terasawa K, Kashihara D, Hirano K, Tani T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun 2013;4:1829.
23. Miletta MC, Petkovic V, Eblé A, Ammann RA, Flück CE, Mullis PE. Butyrate increases intracellular calcium levels and enhances growth hormone release from rat anterior pituitary cells via the G-protein-coupled receptors GPR41 and 43. PLoS One 2014;9: e107388.
24. Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 2003; 278:25481-25489.
25. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003; 278:11312-11319.
26. Fusunyan RD, Quinn JJ, Fujimoto M, MacDermott RP, Sanderson IR. Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Mol Med 1999;5: 631-640.
27. Mirković B, Murray M, Lavelle G, Bergin DA, Devery R, Greene CM, McElvaney NG. Role of short chain fatty acids, produced by anaerobic bacteria, in the cystic fibrosis airway [abstract]. Am J Respir Crit Care Med 2013;187: A5285.
28. Mirković B, Murray M, Lavelle GM, Devery R, Molloy K, Greene CM, McElvaney NG. Short chain fatty acids, produced by anaerobic bacteria, elicit a pro-inflammatory response in the cystic fibrosis airway [abstract]. Am J Respir Crit Care Med 2014;189: A1718.
29. Mirković B, Murray MA, Lavelle GM, Molloy K, Gunaratnam C, Devery R, Greene CM, McElvaney NG. Short chain fatty acids, produced by anaerobic bacteria, elicit a pro-inflammatory response in the cystic fibrosis airway [abstract]. Am J Respir Crit Care Med 2015;191: A3803.
30. Oglesby IK, Bray IM, Chotirmall SH, Stallings RL, O'Neill SJ, McElvaney NG, Greene CM. miR-126 is downregulated in cystic fibrosis airway epithelial cells and regulates TOM1 expression. J Immunol 2010;184: 1702-1709.
31. Bergin DA, Hurley K, Mehta A, Cox S, Ryan D, O'Neill SJ, Reeves EP, McElvaney NG. Airway inflammatory markers in individuals with cystic fibrosis and non-cystic fibrosis bronchiectasis. J Inflamm Res 2013;6:1-11.
32. Bartoszewski R, Rab A, Jurkuvenaite A, Mazur M, Wakefield J, Collawn JF, Bebok Z. Activation of the unfolded protein response by DF508 CFTR. Am J Respir Cell Mol Biol 2008;39:448-457.
33. Oslowski CM, Urano F. Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol 2011;490:71-92.
34. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014;20:159-166.
35. Cohen-Cymberknoh M, Kerem E, Ferkol T, Elizur A. Airway inflammation in cystic fibrosis: molecular mechanisms and clinical implications. Thorax 2013;68:1157-1162.
36. Cosgrove S, Chotirmall SH, Greene CM, McElvaney NG. Pulmonary proteases in the cystic fibrosis lung induce interleukin 8 expression from bronchial epithelial cells via a heme/meprin/epidermal growth factor receptor/Toll-like receptor pathway. J Biol Chem 2011;286: 7692-7704.
37. Greene CM, Carroll TP, Smith SGJ, Taggart CC, Devaney J, Griffin S, O'Neill SJ, McElvaney NG. TLR-induced inflammation in cystic fibrosis and non-cystic fibrosis airway epithelial cells. J Immunol 2005;174:1638-1646.
38. Walsh DE, Greene CM, Carroll TP, Taggart CC, Gallagher PM, O'Neill SJ, McElvaney NG. Interleukin-8 up-regulation by neutrophil elastase is mediated by MyD88/IRAK/TRAF-6 in human bronchial epithelium. J Biol Chem 2001;276: 35494-35499.
39. Vinolo MAR, Ferguson GJ, Kulkarni S, Damoulakis G, Anderson K, Bohlooly-Y M, Stephens L, Hawkins PT, Curi R. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor. PLoS One 2011;6: e21205.
40. Vinolo MAR, Hatanaka E, Lambertucci RH, Newsholme P, Curi R. Effects of short chain fatty acids on effector mechanisms of neutrophils. Cell Biochem Funct 2009;27:48-55.
41. Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 2008;19:587-593.
42. Cutting GR. Cystic fibrosis genetics: from molecular understanding to clinical application. Nat Rev Genet 2015;16:45-56.
43. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA. Org resource: targets and expression. Nucleic Acids Res 2008;36 (Database issue): D149-D153.
44. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010;11: R90.
45. Blohmke CJ, Mayer ML, Tang AC, Hirschfeld AF, Fjell CD, Sze MA, Falsafi R, Wang S, Hsu K, Chilvers MA, et al. Atypical activation of the unfolded protein response in cystic fibrosis airway cells contributes to p38 MAPK-mediated innate immune responses. J Immunol 2012;189:5467-5475.
46. Kerbiriou M, Le Drévo M-A, Férec C, Trouvé P. Coupling cystic fibrosis to endoplasmic reticulum stress: differential role of Grp78 and ATF6. Biochim Biophys Acta 2007;1772: 1236-1249.