Aggregation Substance Promotes Adherence, Phagocytosis, and Intracellular Survival of Enterococcus Faecalis Within Human Macrophages and Suppresses Respiratory Burst

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2000 Aug 19

PMID 10948103

Citations 70

Authors

S D Sussmuth

R Wirth

M Susa

R Marre

E Rozdzinski

Affiliations

Soon will be listed here.

Abstract

The aggregation substance (AS) of Enterococcus faecalis, encoded on sex pheromone plasmids, is a surface-bound glycoprotein that mediates aggregation between bacteria thereby facilitating plasmid transfer. Sequencing of the pAD1-encoded Asa1 revealed that this surface protein contains two RGD motifs which are known to ligate integrins. Therefore, we investigated the influence of AS on the interaction of E. faecalis with human monocyte-derived macrophages which constitutively express beta(2) integrins (e.g., CD18). AS was found to cause a greater-than-fivefold increase in enterococcal adherence to macrophages and a greater-than-sevenfold increase in phagocytosis. Adherence was mediated by an interaction between the RGD motif and the integrin CD11b/CD18 (complement receptor type 3) as demonstrated by inhibition studies with monoclonal antibodies and RGD peptide. AS-bearing enterococci were significantly more resistant to macrophage killing during the first 3 h postinfection, probably due to inhibition of the respiratory burst as indicated by reduced concentrations of superoxide anion.

Citing Articles

Enterococcal-host interactions in the gastrointestinal tract and beyond.

Madani W, Ramos Y, Cubillos-Ruiz J, Morales D FEMS Microbes. 2024; 5:xtae027.

PMID: 39391373 PMC: 11466040. DOI: 10.1093/femsmc/xtae027.

: an overlooked cell invader.

Archambaud C, Nunez N, da Silva R, Kline K, Serror P Microbiol Mol Biol Rev. 2024; 88(3):e0006924.

PMID: 39239986 PMC: 11426025. DOI: 10.1128/mmbr.00069-24.

Comparative Probiogenomics Analysis of Limosilactobacillus fermentum 3872.

Ullah M, Rizwan M, Han J, Raza A, Chen Y, Yan M Probiotics Antimicrob Proteins. 2024; .

PMID: 38717735 DOI: 10.1007/s12602-024-10286-4.

Comparative Analysis of Antibiotic Resistance and Biofilm Characteristics of Two Major Species from Poultry Slaughterhouses in South Korea.

Son Y, Jin Y, Cho E, Park A, Flores R, Nguyen B Vet Sci. 2024; 11(4).

PMID: 38668447 PMC: 11054628. DOI: 10.3390/vetsci11040180.

Structural foundation for the role of enterococcal PrgB in conjugation, biofilm formation, and virulence.

Sun W, Lassinantti L, Jarva M, Schmitt A, Ter Beek J, Berntsson R Elife. 2023; 12.

PMID: 37860966 PMC: 10588982. DOI: 10.7554/eLife.84427.

References

Hogg N, Takacs L, Palmer D, Selvendran Y, Allen C . The p150,95 molecule is a marker of human mononuclear phagocytes: comparison with expression of class II molecules. Eur J Immunol. 1986; 16(3):240-8. DOI: 10.1002/eji.1830160306. View

Vanek N, Simon S, Mariscalco M, Dunny G, Rakita R . Enterococcus faecalis aggregation substance promotes opsonin-independent binding to human neutrophils via a complement receptor type 3-mediated mechanism. FEMS Immunol Med Microbiol. 1999; 26(1):49-60. DOI: 10.1111/j.1574-695X.1999.tb01371.x. View

Bullock W, Wright S . Role of the adherence-promoting receptors, CR3, LFA-1, and p150,95, in binding of Histoplasma capsulatum by human macrophages. J Exp Med. 1987; 165(1):195-210. PMC: 2188258. DOI: 10.1084/jem.165.1.195. View

Rakita R, Vanek N, Mee M, Mariscalco M, Dunny G, Snuggs M . Enterococcus faecalis bearing aggregation substance is resistant to killing by human neutrophils despite phagocytosis and neutrophil activation. Infect Immun. 1999; 67(11):6067-75. PMC: 96994. DOI: 10.1128/IAI.67.11.6067-6075.1999. View

Miller R, GARBUS J, Hornick R . Lack of enhanced oxygen consumption by polymorphonuclear leukocytes on phagocytosis of virulent Salmonella typhi. Science. 1972; 175(4025):1010-1. DOI: 10.1126/science.175.4025.1010. View

Babior B . Oxygen-dependent microbial killing by phagocytes (first of two parts). N Engl J Med. 1978; 298(12):659-68. DOI: 10.1056/NEJM197803232981205. View

Kreutzer D, Dreyfus L, ROBERTSON D . Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus. Infect Immun. 1979; 23(3):737-42. PMC: 414228. DOI: 10.1128/iai.23.3.737-742.1979. View

Leijh P, van den Barselaar M, Daha M, Van Furth R . Stimulation of the intracellular killing of Staphylococcus aureus by monocytes: regulation by immunoglobulin G and complement components C3/C3b and B/Bb. J Immunol. 1982; 129(1):332-7. View

Wright S, Silverstein S . Tumor-promoting phorbol esters stimulate C3b and C3b' receptor-mediated phagocytosis in cultured human monocytes. J Exp Med. 1982; 156(4):1149-64. PMC: 2186805. DOI: 10.1084/jem.156.4.1149. View

10.

Baxter M, Leslie R, Reeves W . The stimulation of superoxide anion production in guinea-pig peritoneal macrophages and neutrophils by phorbol myristate acetate, opsonized zymosan and IgG2-containing soluble immune complexes. Immunology. 1983; 48(4):657-65. PMC: 1454078. View

11.

Densen P, Mandell G . Phagocyte strategy vs. microbial tactics. Rev Infect Dis. 1980; 2(5):817-38. DOI: 10.1093/clinids/2.5.817. View

12.

Ike Y, Craig R, White B, Yagi Y, Clewell D . Modification of Streptococcus faecalis sex pheromones after acquisition of plasmid DNA. Proc Natl Acad Sci U S A. 1983; 80(17):5369-73. PMC: 384257. DOI: 10.1073/pnas.80.17.5369. View

13.

Wright S, Rao P, Van Voorhis W, Craigmyle L, Iida K, Talle M . Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc Natl Acad Sci U S A. 1983; 80(18):5699-703. PMC: 384326. DOI: 10.1073/pnas.80.18.5699. View

14.

Wright S, Silverstein S . Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J Exp Med. 1983; 158(6):2016-23. PMC: 2187185. DOI: 10.1084/jem.158.6.2016. View

15.

Ike Y, Clewell D . Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn917 as an insertional mutagen. J Bacteriol. 1984; 158(3):777-83. PMC: 215509. DOI: 10.1128/jb.158.3.777-783.1984. View

16.

Boyum A . Separation of lymphocytes, granulocytes, and monocytes from human blood using iodinated density gradient media. Methods Enzymol. 1984; 108:88-102. DOI: 10.1016/s0076-6879(84)08076-9. View

17.

Dijkmans B, Leijh P, Braat A, Van Furth R . Effect of bacterial competition on the opsonization, phagocytosis, and intracellular killing of microorganisms by granulocytes. Infect Immun. 1985; 49(1):219-24. PMC: 262082. DOI: 10.1128/iai.49.1.219-224.1985. View

18.

Vieweg R, Leslie R . Soluble immune complex triggering of a respiratory burst in macrophages: the role of complex aggregation at the phagocyte surface. Eur J Immunol. 1987; 17(1):149-51. DOI: 10.1002/eji.1830170126. View

19.

Van Dyke K, Van Scott M, Castranova V . Measurement of phagocytosis and cell-mediated cytotoxicity by chemiluminescence. Methods Enzymol. 1986; 132:498-507. DOI: 10.1016/s0076-6879(86)32035-4. View

20.

De Baetselier P, SCHRAM E . Luminescent bioassays based on macrophage cell lines. Methods Enzymol. 1986; 133:507-30. DOI: 10.1016/0076-6879(86)33087-8. View