Expanded glucose import capability affords Staphylococcus aureus optimized glycolytic flux during infection

mBio

Volumn 7, Issue 3, 2016, Pages

  Vitko, Nicholas P ^a   Grosser, Melinda R ^a   Khatri, Dal ^a   Lance, Thurlow R ^a   Richardson, Anthony R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSUGAR; DISACCHARIDE; FRUCTOSE; GALACTOSE; GLUCOSE; LACTOSE; MALTOSE; MALTOTRIOSE; MANNITOL; MANNOSE; N ACETYLGLUCOSAMINE; N ACETYLMANNOSAMINE; RIBOSE; SORBITOL; SUCROSE; TREHALOSE; TURANOSE; UNCLASSIFIED DRUG; LACTIC ACID DERIVATIVE;

ADAPTATION; ANAEROBIC GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL SKIN DISEASE; CONTROLLED STUDY; FEMALE; GLCA GENE; GLCB GENE; GLCC GENE; GLCU GENE; GLUCOSE TRANSPORT; GLYCOLYSIS; HOST PATHOGEN INTERACTION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOFT TISSUE INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; DISEASE MODEL; FERMENTATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; STAPHYLOCOCCAL SKIN INFECTION;

ANAEROBIOSIS; ANIMALS; DISEASE MODELS, ANIMAL; FERMENTATION; GLUCOSE; LACTATES; MICE; SOFT TISSUE INFECTIONS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCAL SKIN INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84979072468     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00296-16     Document Type: Article

References (49)

1. Graham PL, Lin SX, Larson EL. 2006. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med 144: 318-325. http://dx.doi.org/10.7326/0003-4819-144-5-200603070-00006.
2. Schechter-Perkins EM, Mitchell PM, Murray KA, Rubin-Smith JE, Weir S, Gupta K. 2011. Prevalence and predictors of nasal and extranasal staphylococcal colonization in patients presenting to the emergency department. Ann Emerg Med 57: 492-499. http://dx.doi.org/10.1016/ j.annemergmed.2010.11.024.
3. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O’Boyle C, Danila RN, Lynfield R. 2003. Comparison of community-and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 290: 2976-2984. http://dx.doi.org/10.1001/jama.290.22.2976.
4. Moore CL, Hingwe A, Donabedian SM, Perri MB, Davis SL, Haque NZ, Reyes K, Vager D, Zervos MJ. 2009. Comparative evaluation of epidemiology and outcomes of methicillin-resistant Staphylococcus aureus (MRSA) USA300 infections causing community-and healthcareassociated infections. Int J Antimicrob Agents 34: 148-155. http:// dx.doi.org/10.1016/j.ijantimicag.2009.03.004.
5. Schlievert PM, Shands KN, Dan BB, Schmid GP, Nishimura RD. 1981. Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J Infect Dis 143: 509-516. http://dx.doi.org/10.1093/infdis/143.4.509.
6. Becker K, Heilmann C, Peters G. 2014. Coagulase-negative staphylococci. Clin Microbiol Rev 27: 870-926. http://dx.doi.org/10.1128/ CMR.00109-13.
7. Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L, Mackie K, O’Neill G, Day NP. 2002. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70: 4987-4996. http://dx.doi.org/10.1128/IAI.70.9.4987-4996.2002.
8. Foster TJ, Höök M. 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6: 484-488. http://dx.doi.org/10.1016/S0966-842X(98)01400-0.
9. Otto M. 2014. Science direct Staphylococcus aureus toxins. Curr Opin Microbiol 17: 32-37. http://dx.doi.org/10.1016/j.mib.2013.11.004.
10. Harvey CJ, LeBouf RF, Stefaniak AB. 2010. Formulation and stability of a novel artificial human sweat under conditions of storage and use. Toxicol In Vitro 24: 1790-1796. http://dx.doi.org/10.1016/j.tiv.2010.06.016.
11. Psychogios N, Hau DD, Peng J, Guo AC, Mandal R, Bouatra S, Sinelnikov I, Krishnamurthy R, Eisner R, Gautam B, Young N, Xia J, Knox C, Dong E, Huang P, Hollander Z, Pedersen TL, Smith SR, Bamforth F, Greiner R, McManus B, Newman JW, Goodfriend T, Wishart DS. 2011. The human serum metabolome. PLoS One 6: e16957. http://dx.doi.org/10.1371/journal.pone.0016957.
12. Kutyshenko VP, Molchanov M, Beskaravayny P, Uversky VN, Timchenko MA. 2011. Analyzing and mapping sweat metabolomics by highresolution NMR spectroscopy. PLoS One 6: e28824. http://dx.doi.org/10.1371/journal.pone.0028824.
13. Richardson AR, Libby SJ, Fang FC. 2008. A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 319: 1672-1676. http://dx.doi.org/10.1126/science.1155207.
14. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ, Maile R, Richardson AR. 2013. Functional modularity of the arginine catabolic mobile Element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus. Cell Host Microbe 13: 100-107. http://dx.doi.org/10.1016/j.chom.2012.11.012.
15. Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ, Skaar EP. 2006. Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2: e87. http://dx.doi.org/10.1371/ journal.ppat.0020087.
16. Vitko NP, Spahich NA, Richardson AR. 2015. Glycolytic dependency of high-level nitric oxide resistance and virulence in Staphylococcus aureus. mBio 6: e00045-15. http://dx.doi.org/10.1128/mBio.00045-15.
17. Hammer ND, Skaar EP. 2011. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65: 129-147. http:// dx.doi.org/10.1146/annurev-micro-090110-102851.
18. Peregrín-Alvarez JM, Sanford C, Parkinson J. 2009. The conservation and evolutionary modularity of metabolism. Genome Biol 10: R63. http:// dx.doi.org/10.1186/gb-2009-10-6-r63.
19. Dills SS, Apperson A, Schmidt MR, Saier MH. 1980. Carbohydrate transport in bacteria. Microbiol Res 44: 385-418.
20. Postma PW, Lengeler JW, Jacobson GR. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
21. Kotrba P, Inui M, Yukawa H. 2001. Bacterial phosphotransferase system (PTS) in carbohydrate uptake and control of carbon metabolism. J Biosci Bioeng 92: 502-517. http://dx.doi.org/10.1016/S1389-1723(01)80308-X.
22. Muller LM, Gorter KJ, Hak E, Goudzwaard WL, Schellevis FG, Hoepelman AI, Rutten GE. 2005. Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin Infect Dis 41: 281-288. http://dx.doi.org/10.1086/431587.
23. Egan JB, Morse ML. 1965. Carbohydrate transport in Staphylococcus aureus I. Genetic and biochemical analysis of a pleiotropic transport mutant. Biochim Biophys Acta 97: 310-319. http://dx.doi.org/10.1016/0304-4165(65)90096-6.
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: e00537-12. http://dx.doi.org/10.1128/mBio.00537-12.
25. Garnett JP, Braun D, McCarthy AJ, Farrant MR, Baker EH, Lindsay JA, Baines DL. 2014. Fructose transport-deficient Staphylococcus aureus reveals important role of epithelial glucose transporters in limiting sugar-driven bacterial growth in airway surface liquid. Cell Mol Life Sci 71: 4665-4673. http://dx.doi.org/10.1007/s00018-014-1635-y.
26. Castro R, Neves AR, Fonseca LL, Pool WA, Kok J, Kuipers OP, Santos H. 2009. Characterization of the individual glucose uptake systems of Lactococcus lactis: mannose-PTS, cellobiose-PTS and the novel GlcU permease. Mol Microbiol 71: 795-806. http://dx.doi.org/10.1111/j.1365-2958.2008.06564.x.
27. Jack DL, Yang NM, Saier MH, Jr. 2001. The drug/metabolite transporter superfamily. Eur J Biochem 268: 3620-3639. http://dx.doi.org/10.1046/ j.1432-1327.2001.02265.x.
28. Fowler VG, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, Corey GR, Spelman D, Bradley SF, Barsic B, Pappas PA, Anstrom KJ, Wray D, Fortes CQ, Anguera I, Athan E, Jones P, van der Meer JTM, Elliott TSJ, Levine DP, Bayer AS, ICE MD Investigators. 2005. Staphylococcus aureus endocarditis: a consequence of medical progress. JAMA 293: 3012-3021. http://dx.doi.org/10.1001/jama.293.24.3012.
29. Movahed MR, Hashemzadeh M, Jamal MM. 2007. Increased prevalence of infectious endocarditis in patients with type II diabetes mellitus. J Diabetes Complications 21: 403-406. http://dx.doi.org/10.1016/ j.jdiacomp.2007.07.003.
30. Kourany WM, Miro JM, Moreno A, Corey GR, Pappas P, Abrutyn E, Hoen B, Habib G, Fowler V, Jr., Sexton DJ, Olaison L, Cabell CH, ICE MD Investigators. 2006. Influence of diabetes mellitus on the clinical manifestations and prognosis of infective endocarditis: a report from the International Collaboration on Endocarditis-Merged Database. Scand J Infect Dis 38: 613-619. http://dx.doi.org/10.1080/00365540600617017.
31. Cheng S-C, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, Giamarellos-Bourboulis EJ, Martens JH, Rao NA, Aghajanirefah A, Manjeri GR, Li Y, Ifrim DC, Arts RJW, van der Veer BM, Deen PMT, Logie C, O’Neill LA, Willems P, van de Veerdonk FL, van der Meer JWM, Ng A, Joosten LAB, Wijmenga C, Stunnenberg HG, Xavier RJ, Netea MG. 2014. mTOR-and HIF-1-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345: 1250684. http://dx.doi.org/10.1126/science.1250684.
32. Seidl K, Müller S, François P, Kriebitzsch C, Schrenzel J, Engelmann S, Bischoff M, Berger-Bächi B. 2009. Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95. http:// dx.doi.org/10.1186/1471-2180-9-95.
33. Seidl K, Goerke C, Wolz C, Mack D, Berger-Bächi B, Bischoff M. 2008. Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76: 2044-2050. http://dx.doi.org/10.1128/IAI.00035-08.
34. Seidl K, Bischoff M, Berger-Bächi B. 2008. CcpA mediates the catabolite repression of tst in Staphylococcus aureus. Infect Immun 76: 5093-5099. http://dx.doi.org/10.1128/IAI.00724-08.
35. Duncan JL, Cho GJ. 1972. Production of staphylococcal alpha toxin. II. Glucose repression of toxin formation. Infect Immun 6: 689-694.
36. Regassa LB, Novick RP, Betley MJ. 1992. Glucose and nonmaintained pH decrease expression of the accessory gene regulator (agr) in Staphylococcus aureus. Infect Immun 60: 3381-3388.
37. Pelz A, Wieland K-P, Putzbach K, Hentschel P, Albert K, Götz F. 2005. Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J Biol Chem 280: 32493-32498. http://dx.doi.org/10.1074/ jbc.M505070200.
38. Katzif S, Lee EH, Law AB, Tzeng YL, Shafer WM. 2005. CspA regulates pigment production in Staphylococcus aureus through a SigB-dependent mechanism. J Bacteriol 187: 8181-8184. http://dx.doi.org/10.1128/ JB.187.23.8181-8184.2005.
39. Hammer ND, Reniere ML, Cassat JE, Zhang Y, Hirsch AO, Indriati Hood M, Skaar EP. 2013. Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. mBio 4: e00241-13. http://dx.doi.org/10.1128/mBio.00241-13.
40. Pishchany G, McCoy AL, Torres VJ, Krause JC, Crowe JE, Jr., Fabry ME, Skaar EP. 2010. Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8: 544-550. http:// dx.doi.org/10.1016/j.chom.2010.11.002.
41. Spahich NA, Vitko NP, Thurlow LR, Temple B, Richardson AR. 5 February 2016. Staphylococcus aureus lactate-and malate-quinone oxidoreductases contribute to nitric oxide resistance and virulence. Mol Microbiol. http://dx.doi.org/10.1111/mmi.13347.
42. Kinkel TL, Roux CM, Dunman PM, Fang FC. 2013. The Staphylococcus aureus SrrAB two-component system promotes resistance to nitrosative stress and hypoxia. mBio 4: e00696-13. http://dx.doi.org/10.1128/ mBio.00696-13.
43. Reniere ML, Skaar EP. 2008. Staphylococcus aureus haem oxygenases are differentially regulated by iron and haem. Mol Microbiol 69: 1304-1315. http://dx.doi.org/10.1111/j.1365-2958.2008.06363.x.
44. Chu VH, Cabell CH, Benjamin DK, Kuniholm EF, Fowler VG, Engemann J, Sexton DJ, Corey GR, Wang A. 2004. Early predictors of in-Hospital death in infective endocarditis. Circulation 109: 1745-1749. http://dx.doi.org/10.1161/01.CIR.0000124719.61827.7F.
45. Lipsky BA, Tabak YP, Johannes RS, Vo L, Hyde L, Weigelt JA. 2010. Skin and soft tissue infections in hospitalised patients with diabetes: culture isolates and risk factors associated with mortality, length of stay and cost. Diabetologia 53: 914-923. http://dx.doi.org/10.1007/s00125-010-1672-5.
46. Federspiel JJ, Stearns SC, Peppercorn AF, Chu VH, Fowler VG. 2012. Increasing US rates of endocarditis with Staphylococcus aureus: 1999-2008. Arch Intern Med 172: 363-365. http://dx.doi.org/10.1001/ archinternmed.2011.1027.
47. Kumar NS, Dullaghan EM, Finlay BB, Gong H, Reiner NE, Jon Paul Selvam J, Thorson LM, Campbell S, Vitko N, Richardson AR, Zoraghi R, YoungRN. 2014. Discovery and optimization of a new class of pyruvate kinase inhibitors as potential therapeutics for the treatment of methicillinresistant Staphylococcus aureus infections. Bioorg Med Chem 22: 1708-1725. http://dx.doi.org/10.1016/j.bmc.2014.01.020.
48. Vitko NP, Richardson AR. 2013. Laboratory maintenance of methicillinresistant Staphylococcus aureus (MRSA). Curr Protoc Microbiol Chapter 9: Unit 9C.2. http://dx.doi.org/10.1002/9780471729259.mc09c02s28.
49. Crooke AK, Fuller JR, Obrist MW, Tomkovich SE, Vitko NP, Richardson AR. 2013. CcpA-independent glucose regulation of lactate dehydrogenase 1 in Staphylococcus aureus. PLoS One 8: e54293. http://dx.doi.org/10.1371/journal.pone.0054293.