Streptococcus pneumoniae in the heart subvert the host response through biofilm-mediated resident macrophage killing

PLoS Pathogens

Volumn 13, Issue 8, 2017, Pages

  Shenoy, Anukul T ^a,b   Brissac, Terry ^a   Gilley, Ryan P ^b   Kumar, Nikhil ^c   Wang, Yong ^d   Gonzalez Juarbe, Norberto ^a   Hinkle, Whitney S ^a   Daugherty, Sean C ^c   Shetty, Amol C ^c   Ott, Sandra ^c   Tallon, Luke J ^c   Deshane, Jessy ^d   Tettelin, Hervé ^c   Orihuela, Carlos J ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LACTATE DEHYDROGENASE; PNEUMOLYSIN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BIOFILM; CARDIAC MUSCLE; CELL ADHESION ASSAY; CELL KILLING; CYTOTOXICITY ASSAY; EXTRACELLULAR MATRIX; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PLANKTON; PRINCIPAL COMPONENT ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; STREPTOCOCCUS PNEUMONIAE; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR ENDOTHELIAL CELL; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; MICROBIOLOGY; MYOCARDITIS; PNEUMOCOCCAL INFECTION; VIRULENCE;

ANIMALS; BIOFILMS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; MACROPHAGES; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; MYOCARDITIS; PNEUMOCOCCAL INFECTIONS; PRINCIPAL COMPONENT ANALYSIS; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTOME; VIRULENCE;

EID: 85028670404     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006582     Document Type: Article

References (62)

1. Corrales-Medina VF, Musher DM, Wells GA, Chirinos JA, Chen L, Fine MJ, Cardiac complications in patients with community-acquired pneumonia: incidence, timing, risk factors, and association with short-term mortality. Circulation. 2012;125(6):773–81. doi: 10.1161/CIRCULATIONAHA.111.040766 22219349.
2. Corrales-Medina VF, Suh KN, Rose G, Chirinos JA, Doucette S, Cameron DW, et al. Cardiac complications in patients with community-acquired pneumonia: a systematic review and meta-analysis of observational studies. PLoS Med. 2011;8(6):e1001048. doi: 10.1371/journal.pmed.1001048 21738449; PubMed Central PMCID: PMCPMC3125176.
3. Valles J, Diaz E, Martin-Loeches I, Bacelar N, Saludes P, Lema J, et al. Evolution over a 15-year period of the clinical characteristics and outcomes of critically ill patients with severe community-acquired pneumonia. Med Intensiva. 2015. doi: 10.1016/j.medin.2015.07.005 26391738.
4. Musher DM, Rueda AM, Kaka AS, Mapara SM, The association between pneumococcal pneumonia and acute cardiac events. Clin Infect Dis. 2007;45(2):158–65. doi: 10.1086/518849 17578773.
5. Eurich DT, Marrie TJ, Minhas-Sandhu JK, Majumdar SR, Risk of heart failure after community acquired pneumonia: prospective controlled study with 10 years of follow-up. BMJ. 2017;356:j413. doi: 10.1136/bmj.j413 28193610.
6. Brown AO, Mann B, Gao G, Hankins JS, Humann J, Giardina J, et al. Streptococcus pneumoniae translocates into the myocardium and forms unique microlesions that disrupt cardiac function. PLoS Pathog. 2014;10(9):e1004383. doi: 10.1371/journal.ppat.1004383 25232870; PubMed Central PMCID: PMCPMC4169480.
7. Gilley RP, Gonzalez-Juarbe N, Shenoy AT, Reyes LF, Dube PH, Restrepo MI, et al. Infiltrated macrophages die of pneumolysin-mediated necroptosis following pneumococcal myocardial invasion. Infection and immunity. 2016. doi: 10.1128/IAI.00007-16 26930705.
8. Alhamdi Y, Neill DR, Abrams ST, Malak HA, Yahya R, Barrett-Jolley R, et al. Circulating Pneumolysin Is a Potent Inducer of Cardiac Injury during Pneumococcal Infection. PLoS Pathog. 2015;11(5):e1004836. doi: 10.1371/journal.ppat.1004836 25973949; PubMed Central PMCID: PMCPMC4431880.
9. Reyes LF, Restrepo MI, Hinojosa CA, Soni NJ, Anzueto A, Babu BL, et al. Severe Pneumococcal Pneumonia Causes Acute Cardiac Toxicity and Subsequent Cardiac Remodeling. Am J Respir Crit Care Med. 2017. doi: 10.1164/rccm.201701-0104OC 28614669.
10. Gilley RP, Orihuela CJ, Pneumococci in biofilms are non-invasive: implications on nasopharyngeal colonization. Front Cell Infect Microbiol. 2014;4:163. doi: 10.3389/fcimb.2014.00163 25414838; PubMed Central PMCID: PMCPMC4222220.
11. Hall-Stoodley L, Hu FZ, Gieseke A, Nistico L, Nguyen D, Hayes J, et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA. 2006;296(2):202–11. doi: 10.1001/jama.296.2.202 16835426; PubMed Central PMCID: PMCPMC1885379.
12. Costerton JW, Stewart PS, Greenberg EP, Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22. 10334980. 10334980
13. Hall-Stoodley L, Nistico L, Sambanthamoorthy K, Dice B, Nguyen D, Mershon WJ, et al. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol. 2008;8:173. doi: 10.1186/1471-2180-8-173 18842140; PubMed Central PMCID: PMCPMC2600794.
14. Moscoso M, Garcia E, Lopez R, Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol. 2006;188(22):7785–95. doi: 10.1128/JB.00673-06 16936041; PubMed Central PMCID: PMCPMC1636320.
15. Blanchette-Cain K, Hinojosa CA, Akula Suresh Babu R, Lizcano A, Gonzalez-Juarbe N, Munoz-Almagro C, et al. Streptococcus pneumoniae biofilm formation is strain dependent, multifactorial, and associated with reduced invasiveness and immunoreactivity during colonization. MBio. 2013;4(5):e00745–13. doi: 10.1128/mBio.00745-13 24129258; PubMed Central PMCID: PMCPMC3812715.
16. Marks LR, Davidson BA, Knight PR, Hakansson AP, Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease. MBio. 2013;4(4). doi: 10.1128/mBio.00438-13 23882016; PubMed Central PMCID: PMCPMC3735180.
17. Shenoy AT, Orihuela CJ, Anatomical site-specific contributions of pneumococcal virulence determinants. Pneumonia (Nathan). 2016;8. doi: 10.1186/s41479-016-0007-9 27635368; PubMed Central PMCID: PMCPMC5021320.
18. Dalia AB, Weiser JN, Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe. 2011;10(5):486–96. doi: 10.1016/j.chom.2011.09.009 22100164; PubMed Central PMCID: PMCPMC3222866.
19. Sanchez CJ, Kumar N, Lizcano A, Shivshankar P, Dunning Hotopp JC, Jorgensen JH, et al. Streptococcus pneumoniae in biofilms are unable to cause invasive disease due to altered virulence determinant production. PLoS One. 2011;6(12):e28738. Epub 2011/12/17. doi: 10.1371/journal.pone.0028738 22174882; PubMed Central PMCID: PMC3234282.
20. Blanchette KA, Shenoy AT, Milner J, 2ndGilley RP, McClure E, Hinojosa CA, et al. Neuraminidase A exposed galactose promotes Streptococcus pneumoniae biofilm formation during colonization. Infection and immunity. 2016. doi: 10.1128/IAI.00277-16 27481242.
21. Weiser JN, Austrian R, Sreenivasan PK, Masure HR, Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infection and immunity. 1994;62(6):2582–9. 8188381; PubMed Central PMCID: PMCPMC186548.
22. Kim JO, Romero-Steiner S, Sorensen UB, Blom J, Carvalho M, Barnard S, et al. Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infection and immunity. 1999;67(5):2327–33. 10225891; PubMed Central PMCID: PMCPMC115974.
23. Kim JO, Weiser JN, Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J Infect Dis. 1998;177(2):368–77. 9466523.
24. Tettelin H, Hollingshead S. K, Tuomanen E I, Mitchell T, Morrison D A, Spratt B G, Comparative genomics of Streptococcus pneumoniae: intrastrain diversity and genome plasticity, p. 15–29. In (ed), The pneumococcus ASM Press, Washington, DC. 2004.
25. Embry A, Hinojosa E, Orihuela CJ, Regions of Diversity 8, 9 and 13 contribute to Streptococcus pneumoniae virulence. BMC Microbiol. 2007;7:80. doi: 10.1186/1471-2180-7-80 17723151; PubMed Central PMCID: PMCPMC2045101.
26. Brown JS, Gilliland SM, Holden DW, A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol. 2001;40(3):572–85. 11359564.
27. Brown JS, Gilliland SM, Basavanna S, Holden DW, phgABC, a three-gene operon required for growth of Streptococcus pneumoniae in hyperosmotic medium and in vivo. Infection and immunity. 2004;72(8):4579–88. doi: 10.1128/IAI.72.8.4579-4588.2004 15271918; PubMed Central PMCID: PMCPMC470583.
28. Brown JS, Gilliland SM, Spratt BG, Holden DW, A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infection and immunity. 2004;72(3):1587–93. doi: 10.1128/IAI.72.3.1587-1593.2004 14977965; PubMed Central PMCID: PMCPMC356060.
29. Majchrzykiewicz JA, Lubelski J, Moll GN, Kuipers A, Bijlsma JJ, Kuipers OP, et al. Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrob Agents Chemother. 2010;54(4):1498–505. doi: 10.1128/AAC.00883-09 20100873; PubMed Central PMCID: PMCPMC2849381.
30. Bayles KW, The biological role of death and lysis in biofilm development. Nat Rev Microbiol. 2007;5(9):721–6. doi: 10.1038/nrmicro1743 17694072.
31. Houldsworth S, Andrew PW, Mitchell TJ, Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-1 beta by human mononuclear phagocytes. Infection and immunity. 1994;62(4):1501–3. 8132361; PubMed Central PMCID: PMCPMC186313.
32. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, Thompson CM, et al. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A. 2003;100(4):1966–71. doi: 10.1073/pnas.0435928100 12569171; PubMed Central PMCID: PMCPMC149942.
33. McNeela EA, Burke A, Neill DR, Baxter C, Fernandes VE, Ferreira D, et al. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog. 2010;6(11):e1001191. doi: 10.1371/journal.ppat.1001191 21085613; PubMed Central PMCID: PMCPMC2978728.
34. Lemon JK, Weiser JN, Degradation products of the extracellular pathogen Streptococcus pneumoniae access the cytosol via its pore-forming toxin. MBio. 2015;6(1). doi: 10.1128/mBio.02110-14 25604786; PubMed Central PMCID: PMCPMC4313911.
35. Thornton RB, Rigby PJ, Wiertsema SP, Filion P, Langlands J, Coates HL, et al. Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr. 2011;11:94. doi: 10.1186/1471-2431-11-94 22018357; PubMed Central PMCID: PMCPMC3224757.
36. Nistico L, Kreft R, Gieseke A, Coticchia JM, Burrows A, Khampang P, et al. Adenoid reservoir for pathogenic biofilm bacteria. J Clin Microbiol. 2011;49(4):1411–20. doi: 10.1128/JCM.00756-10 21307211; PubMed Central PMCID: PMCPMC3122793.
37. Radin JN, Orihuela CJ, Murti G, Guglielmo C, Murray PJ, Tuomanen EI, beta-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae. Infection and immunity. 2005;73(12):7827–35. doi: 10.1128/IAI.73.12.7827-7835.2005 16299272; PubMed Central PMCID: PMCPMC1307033.
38. O'Seaghdha M, Wessels MR, Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from Xenophagic killing. PLoS Pathog. 2013;9(6):e1003394. doi: 10.1371/journal.ppat.1003394 23762025; PubMed Central PMCID: PMCPMC3675196.
39. Hatcher BL, Hale JY, Briles DE, Free Sialic Acid Acts as a Signal That Promotes Streptococcus pneumoniae Invasion of Nasal Tissue and Nonhematogenous Invasion of the Central Nervous System. Infection and immunity. 2016;84(9):2607–15. doi: 10.1128/IAI.01514-15 27354445; PubMed Central PMCID: PMCPMC4995916.
40. Huang ST, Lin CL, Chang YJ, Sher YP, Wu MJ, Shu KH, et al. Pneumococcal pneumonia infection is associated with end-stage renal disease in adult hospitalized patients. Kidney Int. 2014;86(5):1023–30. doi: 10.1038/ki.2014.79 24694991.
41. Shak JR, Ludewick HP, Howery KE, Sakai F, Yi H, Harvey RM, et al. Novel role for the Streptococcus pneumoniae toxin pneumolysin in the assembly of biofilms. MBio. 2013;4(5):e00655–13. doi: 10.1128/mBio.00655-13 24023386; PubMed Central PMCID: PMCPMC3774193.
42. Jensch I, Gamez G, Rothe M, Ebert S, Fulde M, Somplatzki D, et al. PavB is a surface-exposed adhesin of Streptococcus pneumoniae contributing to nasopharyngeal colonization and airways infections. Mol Microbiol. 2010;77(1):22–43. doi: 10.1111/j.1365-2958.2010.07189.x 20444103.
43. Wang J, Karra R, Dickson AL, Poss KD, Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol. 2013;382(2):427–35. doi: 10.1016/j.ydbio.2013.08.012 23988577; PubMed Central PMCID: PMCPMC3852765.
44. Mukerji R, Mirza S, Roche AM, Widener RW, Croney CM, Rhee DK, et al. Pneumococcal surface protein A inhibits complement deposition on the pneumococcal surface by competing with the binding of C-reactive protein to cell-surface phosphocholine. J Immunol. 2012;189(11):5327–35. doi: 10.4049/jimmunol.1201967 23105137; PubMed Central PMCID: PMCPMC3517878.
45. Walker MM, Novak L, Widener R, Grubbs JA, King J, Hale JY, et al. PcpA Promotes Higher Levels of Infection and Modulates Recruitment of Myeloid-Derived Suppressor Cells during Pneumococcal Pneumonia. J Immunol. 2016;196(5):2239–48. doi: 10.4049/jimmunol.1402518 26829988; PubMed Central PMCID: PMCPMC4761482.
46. Hoover SE, Perez AJ, Tsui HC, Sinha D, Smiley DL, DiMarchi RD, et al. A new quorum-sensing system (TprA/PhrA) for Streptococcus pneumoniae D39 that regulates a lantibiotic biosynthesis gene cluster. Mol Microbiol. 2015;97(2):229–43. doi: 10.1111/mmi.13029 25869931; PubMed Central PMCID: PMCPMC4676566.
47. Slamti L, Lereclus D, A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 2002;21(17):4550–9. doi: 10.1093/emboj/cdf450 12198157; PubMed Central PMCID: PMCPMC126190.
48. Hsueh YH, Somers EB, Lereclus D, Wong AC, Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator. Appl Environ Microbiol. 2006;72(7):5089–92. doi: 10.1128/AEM.00573-06 16820512; PubMed Central PMCID: PMCPMC1489338.
49. Perez-Pascual D, Monnet V, Gardan R, Bacterial Cell-Cell Communication in the Host via RRNPP Peptide-Binding Regulators. Front Microbiol. 2016;7:706. doi: 10.3389/fmicb.2016.00706 27242728; PubMed Central PMCID: PMCPMC4873490.
50. Hotomi M, Yuasa J, Briles DE, Yamanaka N, Pneumolysin plays a key role at the initial step of establishing pneumococcal nasal colonization. Folia Microbiol (Praha). 2016;61(5):375–83. doi: 10.1007/s12223-016-0445-z 26803756.
51. Rai P, He F, Kwang J, Engelward BP, Chow VT, Pneumococcal Pneumolysin Induces DNA Damage and Cell Cycle Arrest. Sci Rep. 2016;6:22972. doi: 10.1038/srep22972 27026501; PubMed Central PMCID: PMCPMC4812240.
52. Bogaardt C, van Tonder AJ, Brueggemann AB, Genomic analyses of pneumococci reveal a wide diversity of bacteriocins—including pneumocyclicin, a novel circular bacteriocin. BMC Genomics. 2015;16:554. doi: 10.1186/s12864-015-1729-4 26215050; PubMed Central PMCID: PMCPMC4517551.
53. Briles DE, Tart RC, Swiatlo E, Dillard JP, Smith P, Benton KA, et al. Pneumococcal diversity: considerations for new vaccine strategies with emphasis on pneumococcal surface protein A (PspA). Clin Microbiol Rev. 1998;11(4):645–57. 9767061; PubMed Central PMCID: PMCPMC88902.
54. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001;293(5529):498–506. Epub 2001/07/21. doi: 10.1126/science.1061217 11463916.
55. Kushida H, Propylene oxide as a dehydrating agent for embedding with epoxy resins. Journal of Electron Microscopy. 1961;10(3), 203–204.
56. Weiser JN, Markiewicz Z, Tuomanen EI, Wani JH, Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae. Infection and immunity. 1996;64(6):2240–5. 8675333; PubMed Central PMCID: PMCPMC174062.
57. Garcia-Castillo M, Morosini MI, Valverde A, Almaraz F, Baquero F, Canton R, et al. Differences in biofilm development and antibiotic susceptibility among Streptococcus pneumoniae isolates from cystic fibrosis samples and blood cultures. The Journal of antimicrobial chemotherapy. 2007;59(2):301–4. doi: 10.1093/jac/dkl482 17142818.
58. Kharat AS, Tomasz A, Inactivation of the srtA gene affects localization of surface proteins and decreases adhesion of Streptococcus pneumoniae to human pharyngeal cells in vitro. Infection and immunity. 2003;71(5):2758–65. doi: 10.1128/IAI.71.5.2758-2765.2003 12704150; PubMed Central PMCID: PMC153252.
59. Anders S, Pyl PT, Huber W, HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. doi: 10.1093/bioinformatics/btu638 25260700; PubMed Central PMCID: PMCPMC4287950.
60. Anders S, Huber W, Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106. doi: 10.1186/gb-2010-11-10-r106 20979621; PubMed Central PMCID: PMCPMC3218662.
61. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45. doi: 10.1101/gr.092759.109 19541911; PubMed Central PMCID: PMCPMC2752132.
62. Wessel D, Flugge UI, A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138(1):141–3. 6731838.