Differential interactions of Streptococcus gordonii and Staphylococcus aureus with cultured osteoblasts

Catherine Ella Jauregui, J. P. Mansell, M. A. Jepson, H. F. Jenkinson

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Summary: The impedance of normal osteoblast function by microorganisms is at least in part responsible for the failure of dental or orthopedic implants. Staphylococcus aureus is a major pathogen of bone, and exhibits high levels of adhesion and invasion of osteoblasts. In this article we show that the commensal oral bacterium Streptococcus gordonii also adheres to and is internalized by osteoblasts. Entry of S. gordonii cells had typical features of phagocytosis, similar to S. aureus, with membrane protrusions characterizing initial uptake, and closure of the osteoblast membrane leading to engulfment. The sensitivities of S. gordonii internalization to inhibitors cytochalasin D, colchicine and monensin indicated uptake through endocytosis, with requirement for actin accumulation. Internalization levels of S. gordonii were enhanced by expression of S. aureus fibronectin-binding protein A (FnBPA) on the S. gordonii cell surface. Lysosomal-associated membrane protein-1 phagosomal membrane marker accumulated with intracellular S. aureus and S. gordonii FnBPA, indicating trafficking of bacteria into the late endosomal/lysosomal compartment. Streptococcus gordonii cells did not survive intracellularly for more than 12 h, unless expressing FnBPA, whereas S. aureus showed extended survival times (>48 h). Both S. aureus and S. gordonii DL-1 elicited a rapid interleukin-8 response by osteoblasts, whereas S. gordonii FnBPA was slower. Only S. aureus elicited an interleukin-6 response. Hence, S. gordonii invades osteoblasts by a mechanism similar to that exhibited by S. aureus, and elicits a proinflammatory response that may promote bone resorption.

Original languageEnglish (US)
Pages (from-to)250-266
Number of pages17
JournalMolecular Oral Microbiology
Volume28
Issue number4
DOIs
StatePublished - Aug 1 2013
Externally publishedYes

Fingerprint

Streptococcus gordonii
Osteoblasts
Staphylococcus aureus
Lysosomal-Associated Membrane Protein 1
Membranes
Bacteria
Cytochalasin D
Monensin
Colchicine
Bone Resorption
Endocytosis
Electric Impedance
Interleukin-8
Phagocytosis
Orthopedics
Actins
Interleukin-6
Tooth

Keywords

  • Adherence
  • Cytokine
  • Endocytosis
  • Fibronectin
  • Lysosome

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Dentistry(all)
  • Microbiology (medical)

Cite this

Differential interactions of Streptococcus gordonii and Staphylococcus aureus with cultured osteoblasts. / Jauregui, Catherine Ella; Mansell, J. P.; Jepson, M. A.; Jenkinson, H. F.

In: Molecular Oral Microbiology, Vol. 28, No. 4, 01.08.2013, p. 250-266.

Research output: Contribution to journalArticle

@article{40789801adb940d38058361d96a1f90a,
title = "Differential interactions of Streptococcus gordonii and Staphylococcus aureus with cultured osteoblasts",
abstract = "Summary: The impedance of normal osteoblast function by microorganisms is at least in part responsible for the failure of dental or orthopedic implants. Staphylococcus aureus is a major pathogen of bone, and exhibits high levels of adhesion and invasion of osteoblasts. In this article we show that the commensal oral bacterium Streptococcus gordonii also adheres to and is internalized by osteoblasts. Entry of S. gordonii cells had typical features of phagocytosis, similar to S. aureus, with membrane protrusions characterizing initial uptake, and closure of the osteoblast membrane leading to engulfment. The sensitivities of S. gordonii internalization to inhibitors cytochalasin D, colchicine and monensin indicated uptake through endocytosis, with requirement for actin accumulation. Internalization levels of S. gordonii were enhanced by expression of S. aureus fibronectin-binding protein A (FnBPA) on the S. gordonii cell surface. Lysosomal-associated membrane protein-1 phagosomal membrane marker accumulated with intracellular S. aureus and S. gordonii FnBPA, indicating trafficking of bacteria into the late endosomal/lysosomal compartment. Streptococcus gordonii cells did not survive intracellularly for more than 12 h, unless expressing FnBPA, whereas S. aureus showed extended survival times (>48 h). Both S. aureus and S. gordonii DL-1 elicited a rapid interleukin-8 response by osteoblasts, whereas S. gordonii FnBPA was slower. Only S. aureus elicited an interleukin-6 response. Hence, S. gordonii invades osteoblasts by a mechanism similar to that exhibited by S. aureus, and elicits a proinflammatory response that may promote bone resorption.",
keywords = "Adherence, Cytokine, Endocytosis, Fibronectin, Lysosome",
author = "Jauregui, {Catherine Ella} and Mansell, {J. P.} and Jepson, {M. A.} and Jenkinson, {H. F.}",
year = "2013",
month = "8",
day = "1",
doi = "10.1111/omi.12022",
language = "English (US)",
volume = "28",
pages = "250--266",
journal = "Molecular Oral Microbiology",
issn = "2041-1006",
publisher = "American Journal of Nursing Company",
number = "4",

}

TY - JOUR

T1 - Differential interactions of Streptococcus gordonii and Staphylococcus aureus with cultured osteoblasts

AU - Jauregui, Catherine Ella

AU - Mansell, J. P.

AU - Jepson, M. A.

AU - Jenkinson, H. F.

PY - 2013/8/1

Y1 - 2013/8/1

N2 - Summary: The impedance of normal osteoblast function by microorganisms is at least in part responsible for the failure of dental or orthopedic implants. Staphylococcus aureus is a major pathogen of bone, and exhibits high levels of adhesion and invasion of osteoblasts. In this article we show that the commensal oral bacterium Streptococcus gordonii also adheres to and is internalized by osteoblasts. Entry of S. gordonii cells had typical features of phagocytosis, similar to S. aureus, with membrane protrusions characterizing initial uptake, and closure of the osteoblast membrane leading to engulfment. The sensitivities of S. gordonii internalization to inhibitors cytochalasin D, colchicine and monensin indicated uptake through endocytosis, with requirement for actin accumulation. Internalization levels of S. gordonii were enhanced by expression of S. aureus fibronectin-binding protein A (FnBPA) on the S. gordonii cell surface. Lysosomal-associated membrane protein-1 phagosomal membrane marker accumulated with intracellular S. aureus and S. gordonii FnBPA, indicating trafficking of bacteria into the late endosomal/lysosomal compartment. Streptococcus gordonii cells did not survive intracellularly for more than 12 h, unless expressing FnBPA, whereas S. aureus showed extended survival times (>48 h). Both S. aureus and S. gordonii DL-1 elicited a rapid interleukin-8 response by osteoblasts, whereas S. gordonii FnBPA was slower. Only S. aureus elicited an interleukin-6 response. Hence, S. gordonii invades osteoblasts by a mechanism similar to that exhibited by S. aureus, and elicits a proinflammatory response that may promote bone resorption.

AB - Summary: The impedance of normal osteoblast function by microorganisms is at least in part responsible for the failure of dental or orthopedic implants. Staphylococcus aureus is a major pathogen of bone, and exhibits high levels of adhesion and invasion of osteoblasts. In this article we show that the commensal oral bacterium Streptococcus gordonii also adheres to and is internalized by osteoblasts. Entry of S. gordonii cells had typical features of phagocytosis, similar to S. aureus, with membrane protrusions characterizing initial uptake, and closure of the osteoblast membrane leading to engulfment. The sensitivities of S. gordonii internalization to inhibitors cytochalasin D, colchicine and monensin indicated uptake through endocytosis, with requirement for actin accumulation. Internalization levels of S. gordonii were enhanced by expression of S. aureus fibronectin-binding protein A (FnBPA) on the S. gordonii cell surface. Lysosomal-associated membrane protein-1 phagosomal membrane marker accumulated with intracellular S. aureus and S. gordonii FnBPA, indicating trafficking of bacteria into the late endosomal/lysosomal compartment. Streptococcus gordonii cells did not survive intracellularly for more than 12 h, unless expressing FnBPA, whereas S. aureus showed extended survival times (>48 h). Both S. aureus and S. gordonii DL-1 elicited a rapid interleukin-8 response by osteoblasts, whereas S. gordonii FnBPA was slower. Only S. aureus elicited an interleukin-6 response. Hence, S. gordonii invades osteoblasts by a mechanism similar to that exhibited by S. aureus, and elicits a proinflammatory response that may promote bone resorption.

KW - Adherence

KW - Cytokine

KW - Endocytosis

KW - Fibronectin

KW - Lysosome

UR - http://www.scopus.com/inward/record.url?scp=84880303430&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84880303430&partnerID=8YFLogxK

U2 - 10.1111/omi.12022

DO - 10.1111/omi.12022

M3 - Article

C2 - 23413785

AN - SCOPUS:84880303430

VL - 28

SP - 250

EP - 266

JO - Molecular Oral Microbiology

JF - Molecular Oral Microbiology

SN - 2041-1006

IS - 4

ER -