Differential expression and roles of Staphylococcus aureus virulence determinants during colonization and disease

mBio

Volumn 6, Issue 1, 2015, Pages

  Jenkins, Amy ^a   An Diep, Binh ^b,c   Mai, Thuy T ^b   Vo, Nhung H ^b   Warrener, Paul ^a   Suzich, Joann ^a   Kendall Stover, C ^a   Sellman, Bret R ^a  

^a MEDIMMUNE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; VIRULENCE FACTOR;

ARTICLE; BACTEREMIA; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; FHUD GENE; FNBA GENE; GENE EXPRESSION REGULATION; HLA GENE; IMMUNE EVASION; NONHUMAN; PATHOGENESIS; PHASE TRANSITION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SDRC GENE; SSTD GENE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETICS; HETEROZYGOTE; ISOLATION AND PURIFICATION; MICROBIOLOGY; OSTEOMYELITIS; PATHOGENICITY; PHYSIOLOGY; SEPSIS; SIGMODONTINAE; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANIMALS; CARRIER STATE; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; MICE, INBRED BALB C; OSTEOMYELITIS; SEPSIS; SIGMODONTINAE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

EID: 84924107546     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02272-14     Document Type: Article

References (49)

1. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339: 520-532. http://dx. doi. org/10. 1056/NEJM199808203390806.
2. Kluytmans J, van Belkum A, Verbrugh H. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505-520.
3. Von Eiff C, Becker K, Machka K, Stammer H, Peters G. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med 344: 11-16. http://dx. doi. org/10. 1056/NEJM200101043440102.
4. Lory S, Jin S, Boyd JM, Rakeman JL, Bergman P. 1996. Differential gene expression by Pseudomonas aeruginosa during interaction with respiratory mucus. AmJ Respir Crit Care Med 154: S183-S186. http://dx. doi. org/10. 1164/ajrccm/154. 4_Pt_2. S183.
5. Sitkiewicz I, Babiak I, Hryniewicz W. 2011. Characterization of transcription within sdr region of Staphylococcus aureus. Antonie Van Leeuwenhoek 99: 409-416. http://dx. doi. org/10. 1007/s10482-010-9476-7.
6. Boyce JD, Cullen PA, Adler B. 2004. Genomic-scale analysis of bacterial gene and protein expression in the host. Emerg Infect Dis 10: 1357-1362. http://dx. doi. org/10. 3201/eid1008. 031036.
7. Malachowa N, Whitney AR, Kobayashi SD, Sturdevant DE, Kennedy AD, Braughton KR, Shabb DW, Diep BA, Chambers HF, Otto M, DeLeo FR. 2011. Global changes in Staphylococcus aureus gene expression in human blood. PLoS One 6: e18617. http://dx. doi. org/10. 1371/journal. pone. 0018617.
8. Shemesh M, Tam A, Steinberg D. 2007. Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology 153: 1307-1317. http://dx. doi. org/10. 1099/mic. 0. 2006/002030-0.
9. Goerke C, Fluckiger U, Steinhuber A, Bisanzio V, Ulrich M, Bischoff M, Patti JM, Wolz C. 2005. Role of Staphylococcus aureus global regulators sae and sigma B in virulence gene expression during device-related infection. Infect Immun 73: 3415-3421. http://dx. doi. org/10. 1128/IAI. 73. 6. 3415-3421. 2005.
10. Joost I, Blass D, Burian M, Goerke C, Wolz C, von Müller L, Becker K, Preissner K, Herrmann M, Bischoff M. 2009. Transcription analysis of the extracellular adherence protein from Staphylococcus aureus in authentic human infection and in vitro. J Infect Dis 199: 1471-1478. http://dx. doi. org/10. 1086/598484.
11. Wolz C, Goerke C, Landmann R, Zimmerli W, Fluckiger U. 2002. Transcription of clumping factor A in attached and unattached Staphylococcus aureus in vitro and during device-related infection. Infect Immun 70: 2758-2762. http://dx. doi. org/10. 1128/IAI. 70. 6. 2758-2762. 2002.
12. Loughman JA, Fritz SA, Storch GA, Hunstad DA. 2009. Virulence gene expression in human community-acquired Staphylococcus aureus infection. J Infect Dis 199: 294-301. http://dx. doi. org/10. 1086/595982.
13. Date SV, Modrusan Z, Lawrence M, Morisaki JH, Toy K, Shah IM, Kim J, Park S, Xu M, Basuino L, Chan L, Zeitschel D, Chambers HF, Tan MW, Brown EJ, Diep BA, Hazenbos WL. 2014. Global gene expression of methicillin-resistant Staphylococcus aureus USA300 during human and mouse infection. J Infect Dis 209: 1542-1550. http://dx. doi. org/10. 1093/infdis/jit668.
14. Burian M, Wolz C, Goerke C. 2010. Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS One 5: e10040. http://dx. doi. org/10. 1371/journal. pone. 0010040.
15. Burian M, Rautenberg M, Kohler T, Fritz M, Krismer B, Unger C, Hoffmann WH, Peschel A, Wolz C, Goerke C. 2010. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J Infect Dis 201: 1414-1421. http://dx. doi. org/10. 1086/651619.
16. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, Nicholson G, Neumeister B, Mond JJ, Peschel A. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10: 243-245. http://dx. doi. org/10. 1038/nm991.
17. Schaffer AC, Solinga RM, Cocchiaro J, Portoles M, Kiser KB, Risley A, Randall SM, Valtulina V, Speziale P, Walsh E, Foster T, Lee JC. 2006. Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect Immun 74: 2145-2153. http://dx. doi. org/10. 1128/IAI. 74. 4. 2145-2153. 2006.
18. Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, Acevedo J, Read RC, Day NP, Peacock SJ, Mond JJ, Kokai-Kun JF, Foster SJ. 2006. Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193: 1098-1108. http://dx. doi. org/10. 1086/501471.
19. Kiser KB, Cantey-Kiser JM, Lee JC. 1999. Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect Immun 67: 5001-5006.
20. Kokai-Kun JF, Walsh SM, Chanturiya T, Mond JJ. 2003. Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob Agents Chemother 47: 1589-1597. http://dx. doi. org/10. 1128/AAC. 47. 5. 1589-1597. 2003.
21. Wertheim HF, Walsh E, Choudhurry R, Melles DC, Boelens HA, Miajlovic H, Verbrugh HA, Foster T, van Belkum A. 2008. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med 5: e17. http://dx. doi. org/10. 1371/journal. pmed. 0050017.
22. Corrigan RM, Miajlovic H, Foster TJ. 2009. Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol 9: 22. http://dx. doi. org/10. 1186/1471-2180-9-22.
23. Weidenmaier C, Goerke C, Wolz C. 2012. Staphylococcus aureus determinants for nasal colonization. Trends Microbiol 20: 243-250. http://dx. doi. org/10. 1016/j. tim. 2012. 03. 004.
24. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM, Schneewind O. 2003. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909. http://dx. doi. org/10. 1126/science. 1081147.
25. Andrews SC, Robinson AK, Rodríguez-Quiñones F. 2003. Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237. http://dx. doi. org/10. 1016/S0168-6445(03)00055-X.
26. McAdow M, Kim HK, Dedent AC, Hendrickx AP, Schneewind O, Missiakas DM. 2011. Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 7: e1002307. http://dx. doi. org/10. 1371/journal. ppat. 1002307.
27. Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM. 2009. Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23: 3393-3404. http://dx. doi. org/10. 1096/fj. 09-135467.
28. Menzies BE. 2003. The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections. Curr Opin Infect Dis 16: 225-229. http://dx. doi. org/10. 1097/01. qco. 0000073771. 11390. 75.
29. Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, Yeaman MR, Bayer AS. 2005. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191: 1771-1777. http://dx. doi. org/10. 1086/429692.
30. O'Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ. 2002. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol 4: 759-770. h t t p://d x. d o i. o r g/1 0. 1 0 4 6/j. 1 4 6 2-5822. 2002. 00231. x.
31. Edwards AM, Massey RC, Clarke SR. 2012. Molecular mechanisms of Staphylococcus aureus nasopharyngeal colonization. Mol Oral Microbiol 27: 1-10. http://dx. doi. org/10. 1111/j. 2041-1014. 2011. 00628. x.
32. Barbu EM, Ganesh VK, Gurusiddappa S, Mackenzie RC, Foster TJ, Sudhof TC, Höök M. 2010. Beta-neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog 6: e1000726. http://dx. doi. org/10. 1371/journal. ppat. 1000726.
33. Haley KP, Skaar EP. 2012. A battle for iron: host sequestration and Staphylococcus aureus acquisition. Microbes Infect 14: 217-227. http://dx. doi. org/10. 1016/j. micinf. 2011. 11. 001.
34. Cerca N, Jefferson KK, Maira-Litrán T, Pier DB, Kelly-Quintos C, Goldmann DA, Azeredo J, Pier GB. 2007. Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun 75: 3406-3413. http://dx. doi. org/10. 1128/IAI. 00078-07.
35. Edwards AM, Potts JR, Josefsson E, Massey RC. 2010. Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog 6: e1000964. http://dx. doi. org/10. 1371/journal. ppat. 1000964.
36. Sinha B, François PP, Nüsse O, Foti M, Hartford OM, Vaudaux P, Foster TJ, Lew DP, Herrmann M, Krause KH. 1999. Fibronectinbinding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin 5-1. Cell Microbiol 1: 101-117. http://dx. doi. org/10. 1046/j. 1462-5822. 1999. 00011. x.
37. Roche FM, Massey R, Peacock SJ, Day NP, Visai L, Speziale P, Lam A, Pallen M, Foster TJ. 2003. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 149: 643-654. http://dx. doi. org/10. 1099/mic. 0. 25996-0.
38. Hammer ND, Skaar EP. 2012. The impact of metal sequestration on Staphylococcus aureus metabolism. Curr Opin Microbiol 15: 10-14. http://dx. doi. org/10. 1016/j. mib. 2011. 11. 004.
39. Berube BJ, Bubeck Wardenburg J. 2013. Staphylococcus aureus alphatoxin: nearly a century of intrigue. Toxins (Basel) 5: 1140-1166. http://dx. doi. org/10. 3390/toxins5061140.
40. Patti JM, Höök M. 1994. Microbial adhesins recognizing extracellular matrix macromolecules. Curr Opin Cell Biol 6: 752-758. http://dx. doi. org/10. 1016/0955-0674(94)90104-X.
41. Patti JM, Allen BL, McGavin MJ, Höök M. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48: 585-617. http://dx. doi. org/10. 1146/annurev. mi. 48. 100194. 003101.
42. Bogniard RP, Whipple GH. 1932. The iron content of blood free tissues and viscera. J Exp Med 55: 653-655. http://dx. doi. org/10. 1084/jem. 55. 4. 653.
43. Bayer AS, Ramos MD, Menzies BE, Yeaman MR, Shen AJ, Cheung AL. 1997. Hyperproduction of alpha-toxin by Staphylococcus aureus results in paradoxically reduced virulence in experimental endocarditis: a host defense role for platelet microbicidal proteins. Infect Immun 65: 4652-4660.
44. Powers ME, Kim HK, Wang Y, Bubeck Wardenburg J. 2012. ADAM10 mediates vascular injury induced by Staphylococcus aureus alphahemolysin. J Infect Dis 206: 352-356. http://dx. doi. org/10. 1093/infdis/jis192.
45. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, Jones A, Palazzolo-Ballance AM, Perdreau-Remington F, Sensabaugh GF, DeLeo FR, Chambers HF. 2008. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197: 1523-1530. http://dx. doi. org/10. 1086/587907.
46. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63. http://dx. doi. org/10. 1016/j. plasmid. 2005. 05. 005.
47. Sellman BR, Timofeyeva Y, Nanra J, Scott A, Fulginiti JP, Matsuka YV, Baker SM. 2008. Expression of Staphylococcus epidermidis SdrG increases following exposure to an in vivo environment. Infect Immun 76: 2950-2957. http://dx. doi. org/10. 1128/IAI. 00055-08.
48. Marco ML, Kleerebezem M. 2008. Assessment of real-time RT-PCR for quantification of Lactobacillus plantarum gene expression during stationary phase and nutrient starvation. J Appl Microbiol 104: 587-594. doi http://dx. doi. org/10. 1111/j. 1365-2672. 2007. 03578. x.
49. T) method. Methods 25: 402-408. http://dx. doi. org/10. 1006/meth. 2001. 1262.