Fructose transport-deficient Staphylococcus aureus reveals important role of epithelial glucose transporters in limiting sugar-driven bacterial growth in airway surface liquid

Cellular and Molecular Life Sciences

Volumn 71, Issue 23, 2014, Pages 4665-4673

  Garnett, James P ^a   Braun, Daniela ^a   McCarthy, Alex J ^a   Farrant, Matthew R ^a   Baker, Emma H ^a   Lindsay, Jodi A ^a   Baines, Deborah L ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Airway epithelium; Glucose; Glucose transporters (GLUTs); Hyperglycaemia; Respiratory infection; Staphylococcus aureus

Indexed keywords

BACTERIAL PROTEIN; FRUCTOSE; GLUCOSE; GLUCOSE TRANSPORTER; TRANSPOSON;

CELL LINE; COCULTURE; COMPLICATION; EPITHELIUM CELL; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; HYPERGLYCEMIA; METABOLISM; MICROBIOLOGY; MUTATION; RESPIRATORY TRACT MUCOSA; STAPHYLOCOCCUS AUREUS; TRANSPORT AT THE CELLULAR LEVEL; TRANSPOSON;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL LINE; COCULTURE TECHNIQUES; DNA TRANSPOSABLE ELEMENTS; EPITHELIAL CELLS; FRUCTOSE; GENE DELETION; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HUMANS; HYPERGLYCEMIA; MONOSACCHARIDE TRANSPORT PROTEINS; MUTATION; RESPIRATORY MUCOSA; STAPHYLOCOCCUS AUREUS;

EID: 84922394858     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1635-y     Document Type: Article

References (44)

1. Baker EH, Janaway CH, Philips BJ, Brennan AL, Baines DL, Wood DM, Jones PW (2006) Hyperglycaemia is associated with poor outcomes in patients admitted to hospital with acute exacerbations of chronic obstructive pulmonary disease. Thorax 61:284-289
2. Philips BJ, Redman J, Brennan A, Wood D, Holliman R, Baines D, Baker EH (2005) Glucose in bronchial aspirates increases the risk of respiratory MRSA in intubated patients. Thorax 60:761-764
3. Tamer A, Karabay O, Ekerbicer H (2006) Staphylococcus aureus nasal carriage and associated factors in type 2 diabetic patients. Jpn J Infect Dis 59:10-14
4. Merlo CA, Boyle MP, Diener-West M, Marshall BC, Goss CH, Lechtzin N (2007) Incidence and risk factors for multiple antibiotic-resistant Pseudomonas aeruginosa in cystic fibrosis. Chest 132:562-568
5. Brennan AL, Gyi KM, Wood DM, Johnson J, Holliman R, Baines DL, Philips BJ, Geddes DM, Hodson ME, Baker EH (2007) Airway glucose concentrations and effect on growth of respiratory pathogens in cystic fibrosis. J Cyst Fibros 6:101-109
6. Kupeli E, Ulubay G, Ulasli SS, Sahin T, Erayman Z, Gursoy A (2010) Metabolic syndrome is associated with increased risk of acute exacerbation of COPD: a preliminary study. Endocrine 38:76-82
7. Barker PM, Boyd CA, Ramsden CA, Strang LB, Walters DV (1989) Pulmonary glucose transport in the fetal sheep. J Physiol 409:15-27
8. Saumon G, Martet G (1996) Effect of changes in paracellular permeability on airspace liquid clearance: role of glucose transport. Am J Physiol 270:L191-L198
9. Baker EH, Clark N, Brennan AL, Fisher DA, Gyi KM, Hodson ME, Philips BJ, Baines DL, Wood DM (2007) Hyperglycemia and cystic fibrosis alter respiratory fluid glucose concentrations estimated by breath condensate analysis. J Appl Physiol 102:1969-1975
10. Philips BJ, Meguer JX, Redman J, Baker EH (2003) Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intensive Care Med 29:2204-2210
11. Wood DM, Brennan AL, Philips BJ, Baker EH (2004) Effect of hyperglycaemia on glucose concentration of human nasal secretions. Clin Sci (Lond) 106:527-533
12. Garnett JP, Nguyen TT, Moffatt JD, Pelham ER, Kalsi KK, Baker EH, Baines DL (2012) Proinflammatory mediators disrupt glucose homeostasis in airway surface liquid. J Immunol 189:373-380
13. Kalsi KK, Baker EH, Fraser O, Chung YL, Mace OJ, Tarelli E, Philips BJ, Baines DL (2009) Glucose homeostasis across human airway epithelial cell monolayers: role of diffusion, transport and metabolism. Pflugers Arch 457:1061-1070
14. Pezzulo AA, Gutierrez J, Duschner KS, McConnell KS, Taft PJ, Ernst SE, Yahr TL, Rahmouni K, Klesney-Tait J, Stoltz DA, Zabner J (2011) Glucose depletion in the airway surface liquid is essential for sterility of the airways. PLoS One 6:e16166
15. Garnett JP, Gray MA, Tarran R, Brodlie M, Ward C, Baker EH, Baines DL (2013) Elevated paracellular glucose flux across cystic fibrosis airway epithelial monolayers is an important factor for Pseudomonas aeruginosa growth. PLoS One 8:e76283
16. Kalsi KK, Baker EH, Medina RA, Rice S, Wood DM, Ratoff JC, Philips BJ, Baines DL (2008) Apical and basolateral localisation of GLUT2 transporters in human lung epithelial cells. Pflugers Arch 456:991-1003
17. Myerburg MM, King JD Jr, Oyster NM, Fitch AC, Magill A, Baty CJ, Watkins SC, Kolls JK, Pilewski JM, Hallows KR (2010) AMPK agonists ameliorate sodium and fluid transport and inflammation in cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 42:676-684
18. Garnett JP, Baker EH, Naik S, Lindsay JA, Knight GM, Gill S, Tregoning JS, Baines DL (2013) Metformin reduces airway glucose permeability and hyperglycaemia-induced Staphylococcus aureus load independently of effects on blood glucose. Thorax 68:835-845
19. Le MT, Frye RF, Rivard CJ, Cheng J, McFann KK, Segal MS, Johnson RJ, Johnson JA (2012) Effects of high-fructose corn syrup and sucrose on the pharmacokinetics of fructose and acute metabolic and hemodynamic responses in healthy subjects. Metabolism 61:641-651
20. Wahjudi PN, Patterson ME, Lim S, Yee JK, Mao CS, Lee WN (2010) Measurement of glucose and fructose in clinical samples using gas chromatography/mass spectrometry. Clin Biochem 43:198-207
21. Sheludiakova A, Rooney K, Boakes RA (2012) Metabolic and behavioural effects of sucrose and fructose/glucose drinks in the rat. Eur J Nutr 51:445-454
22. Stanhope KL, Havel PJ (2010) Fructose consumption: recent results and their potential implications. Ann N Y Acad Sci 1190:15-24
23. Cummings BP, Stanhope KL, Graham JL, Evans JL, Baskin DG, Griffen SC, Havel PJ (2010) Dietary fructose accelerates the development of diabetes in UCD-T2DM rats: amelioration by the antioxidant, alpha-lipoic acid. Am J Physiol Regul Integr Comp Physiol 298:R1343-R1350
24. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW (2013) A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. MBio 4:e00537-e00612
25. Brennan A, Baines D, Woollhead A, Lindsay J, Hayes M, Philips B, Baker E (2006) Development of an in vitro model to investigate the effect of glucose on the interaction between respiratory epithelia and bacterial pathogens. Thorax 61:101
26. Donenko FV, Gruber IM, Semenova IB, Priyatkin RG, Ziganshin RH, Zaryadyeva EA, Ignatova OM, Kurbatova EA, Kiselevsky MV, Efferth T (2011) Growth-dependent release of carbohydrate metabolism-related and antioxidant enzymes from Staphylococcus aureus strain 6 as determined by proteomic analysis. Exp Ther Med 2:1199-1204
27. Strasters KC, Winkler KC (1963) Carbohydrate metabolism of Staphylococcus aureus. J Gen Microbiol 33:213-229
28. Lee RJ, Kofonow JM, Rosen PL, Siebert AP, Chen B, Doghramji L, Xiong G, Adappa ND, Palmer JN, Kennedy DW, Kreindler JL, Margolskee RF, Cohen NA (2014) Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J Clin Invest 124:1393-1405
29. Seidl K, Goerke C, Wolz C, Mack D, Berger-Bachi B, Bischoff M (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76:2044-2050
30. Seidl K, Muller S, Francois P, Kriebitzsch C, Schrenzel J, Engelmann S, Bischoff M, Berger-Bachi B (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9:95
31. Knezevic I, Bachem S, Sickmann A, Meyer HE, Stulke J, Hengstenberg W (2000) Regulation of the glucose-specific phosphotransferase system (PTS) of Staphylococcus carnosus by the antiterminator protein GlcT. Microbiology 146(Pt 9):2333-2342
32. Meadow ND, Saffen DW, Dottin RP, Roseman S (1982) Molecular cloning of the crr gene and evidence that it is the structural gene for IIIGlc, a phosphocarrier protein of the bacterial phosphotransferase system. Proc Natl Acad Sci USA 79:2528-2532
33. Siebold C, Flukiger K, Beutler R, Erni B (2001) Carbohydrate transporters of the bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS). FEBS Lett 504:104-111
34. Curtis SJ, Epstein W (1975) Phosphorylation of d-glucose in Escherichia coli mutants defective in glucose phosphotransferase, mannose phosphotransferase, and glucokinase. J Bacteriol 122:1189-1199
35. Kornberg HL, Jones-Mortimer MC (1975) PtsX: a gene involved in the uptake of glucose and fructose by Escherichia coli. FEBS Lett 51:1-4
36. Plumbridge J (2000) A mutation which affects both the specificity of PtsG sugar transport and the regulation of ptsG expression by Mlc in Escherichia coli. Microbiology 146(Pt 10):2655-2663
37. Garnett JP, Baker EH, Baines DL (2012) Sweet talk - insights into the nature and importance of glucose transport in lung epithelium. Eur Respir J 40:1269-1276
38. Colville CA, Seatter MJ, Jess TJ, Gould GW, Thomas HM (1993) Kinetic analysis of the liver-type (GLUT2) and brain-type (GLUT3) glucose transporters in Xenopus oocytes: substrate specificities and effects of transport inhibitors. Biochem J 290(Pt 3):701-706
39. Cheeseman CI (1993) GLUT2 is the transporter for fructose across the rat intestinal basolateral membrane. Gastroenterology 105:1050-1056
40. Dawson PA, Mychaleckyj JC, Fossey SC, Mihic SJ, Craddock AL, Bowden DW (2001) Sequence and functional analysis of GLUT10: a glucose transporter in the Type 2 diabetes-linked region of chromosome 20q12-13.1. Mol Genet Metab 74:186-199
41. Manolescu AR, Witkowska K, Kinnaird A, Cessford T, Cheeseman C (2007) Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda) 22:234-240
42. Lee YC, Huang HY, Chang CJ, Cheng CH, Chen YT (2010) Mitochondrial GLUT10 facilitates dehydroascorbic acid import and protects cells against oxidative stress: mechanistic insight into arterial tortuosity syndrome. Hum Mol Genet 19:3721-3733
43. Pyla R, Poulose N, Jun JY, Segar L (2013) Expression of conventional and novel glucose transporters, GLUT1, -9, -10, and -12, in vascular smooth muscle cells. Am J Physiol Cell Physiol 304:C574-C589
44. Faiyaz-Ul-Haque M, Zaidi SH, Al-Sanna N, Alswaid A, Momenah T, Kaya N, Al-Dayel F, Bouhoaigah I, Saliem M, Tsui LC, Teebi AS (2009) A novel missense and a recurrent mutation in SLC2A10 gene of patients affected with arterial tortuosity syndrome. Atherosclerosis 203:466-471