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Blood-Retinal Barrier Compromise And Endogenous Staphylococcus Aureus Endophthalmitis.

P. Coburn, B. Wiskur, R. Astley, M. Callegan
Published 2015 · Medicine

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PURPOSE To test the hypothesis that blood-retinal barrier compromise is associated with the development of endogenous Staphylococcus aureus endophthalmitis. METHODS To compromise the blood-retinal barrier in vivo, streptozotocin-induced diabetes was induced in C57BL/6J mice for 1, 3, or 5 months. Diabetic and age-matched nondiabetic mice were intravenously injected with 108 colony-forming units (cfu) of S. aureus, a common cause of endogenous endophthalmitis in diabetics. After 4 days post infection, electroretinography, histology, and bacterial counts were performed. Staphylococcus aureus-induced alterations in in vitro retinal pigment epithelial (RPE) cell barrier structure and function were assessed by anti-ZO-1 immunohistochemistry, FITC-dextran conjugate diffusion, and bacterial transmigration assays. RESULTS We observed one bilateral infection in a control, nondiabetic animal (mean = 1.54 × 103 ± 1.78 × 10² cfu/eye, 7% incidence). Among the 1-month diabetic mice, we observed culture-confirmed unilateral infections in two animals (mean = 5.54 × 10² ± 7.09 × 10² cfu/eye, 12% incidence). Among the 3-month diabetic mice, infections were observed in 11 animals, three with bilateral infections (mean = 2.67 × 10² ± 2.49 × 10² cfu/eye, 58% incidence). Among the 5-month diabetic mice, we observed infections in five animals (mean = 7.88 × 10² ± 1.08 × 10³ cfu/eye, 33% incidence). In vitro, S. aureus infection reduced ZO-1 immunostaining and disrupted the barrier function of cultured RPE cells, resulting in diffusion of fluorophore-conjugated dextrans and transmigration of live bacteria across a permeabilized RPE barrier. CONCLUSIONS Taken together, these results indicated that S. aureus is capable of inducing blood-retinal barrier permeability and causing endogenous bacterial endophthalmitis in normal and diabetic animals.
This paper references
10.1007/s12272-010-1007-6
How to overcome retinal neuropathy: The fight against angiogenesisrelated blindness
D. Jo (2010)
Image processing with ImageJ
M. Abràmoff (2004)
Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesin.
J. Patti (1992)
10.1371/journal.ppat.1000715
Staphylococcus aureus Panton-Valentine Leukocidin Is a Very Potent Cytotoxic Factor for Human Neutrophils
B. Loeffler (2010)
10.1016/0042-6822(67)90105-5
Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus.
R. Novick (1967)
10.1111/J.1574-695X.2007.00350.X
Staphylococcal peptidoglycan initiates an inflammatory response and procoagulant activity in human vascular endothelial cells: a comparison with highly purified lipoteichoic acid and TSST-1.
E. Mattsson (2008)
10.1371/journal.pone.0043046
Staphylococcus aureus Extracellular Adherence Protein Triggers TNFα Release, Promoting Attachment to Endothelial Cells via Protein A
A. M. Edwards (2012)
10.2337/DIABETES.52.2.506
A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat.
V. Asnaghi (2003)
10.1167/iovs.11-7798
Contribution of mucoviscosity-associated gene A (magA) to virulence in experimental Klebsiella pneumoniae endophthalmitis.
J. J. Hunt (2011)
10.1038/nmeth.2089
NIH Image to ImageJ: 25 years of image analysis
C. Schneider (2012)
10.1016/S0002-9440(10)65607-6
Ocular neovascularization: clarifying complex interactions.
K. Neely (1998)
10.1128/IAI.00088-10
Repair of Global Regulators in Staphylococcus aureus 8325 and Comparative Analysis with Other Clinical Isolates
S. Herbert (2010)
10.1016/0039-6257(86)90076-7
Metastatic bacterial endophthalmitis: a contemporary reappraisal.
M. Greenwald (1986)
10.1097/IAE.0b013e3181ecccf0
ENDOGENOUS METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS ENDOPHTHALMITIS
Vincent Ho (2011)
10.1160/TH06-02-0116
Fibronectin binding proteins contribute to the adherence of Staphylococcus aureus to intact endothelium in vivo.
Sylvain Kerdudou (2006)
Accessory gene regulator controls Staphylococcus aureus virulence in endophthalmitis.
M. Booth (1995)
10.1038/182419a0
The Rat
H. Harris (1958)
10.1111/j.1365-2958.1994.tb01271.x
Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria.
W. Navarre (1994)
10.1016/j.ajo.2009.08.023
Staphylococcus aureus endophthalmitis: antibiotic susceptibilities, methicillin resistance, and clinical outcomes.
J. C. Major (2010)
10.1128/IAI.70.8.4697-4700.2002
Internalization of Staphylococcus aureus by Human Corneal Epithelial Cells: Role of Bacterial Fibronectin-Binding Protein and Host Cell Factors
B. Jett (2002)
10.1016/J.OPHTHA.2004.11.045
Vitreous levels of vascular endothelial growth factor and intercellular adhesion molecule 1 are related to diabetic macular edema.
H. Funatsu (2005)
10.1128/IAI.01710-14
Staphylococcus aureus Hyaluronidase Is a CodY-Regulated Virulence Factor
Carolyn B Ibberson (2014)
10.1097/SMJ.0b013e3181b21a40
SAME Is Different: A Case Report and Literature Review of Staphylococcus aureus Metastatic Endophthalmitis
Neil A Nixdorff (2009)
10.1016/s0161-6420(13)31255-x
Endogenous bacterial endophthalmitis. Report of a ten-year retrospective study.
A. Okada (1994)
10.1111/j.1365-2958.1994.tb00304.x
Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus.
D. McDevitt (1994)
10.1128/IAI.68.7.3965-3970.2000
Peptidoglycan and Lipoteichoic Acid from Staphylococcus aureus Induce Tumor Necrosis Factor Alpha, Interleukin 6 (IL-6), and IL-10 Production in Both T Cells and Monocytes in a Human Whole Blood Model
J. Wang (2000)
10.1128/IAI.67.7.3348-3356.1999
Pathogenesis of Gram-Positive Bacterial Endophthalmitis
M. Callegan (1999)
10.1167/iovs.12-10661
The diabetic ocular environment facilitates the development of endogenous bacterial endophthalmitis.
P. Coburn (2012)
Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition
K. Miyarnoto (1999)
10.1167/iovs.08-2276
Hypermucoviscosity as a virulence factor in experimental Klebsiella pneumoniae endophthalmitis.
B. Wiskur (2008)
10.1056/NEJM199808203390806
Staphylococcus aureus infections.
F. Lowy (1998)
10.1167/IOVS.04-1139
Fas ligand but not complement is critical for control of experimental Staphylococcus aureus Endophthalmitis.
M. Engelbert (2005)
10.1080/02713680600976925
Acute Inflammation and Loss of Retinal Architecture and Function During Experimental Bacillus Endophthalmitis
R. T. Ramadan (2006)
10.18388/ABP.2009_2491
Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity.
K. Plata (2009)
VEGF-initiated blood-retinal barrier breakdown in early diabetes.
T. Qaum (2001)
10.1097/IAE.0b013e3181a3b7a1
ENDOGENOUS ENDOPHTHALMITIS CAUSED BY METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS (MRSA)
Thomas Ness (2009)
10.1097/IIO.0b013e3181d26dfc
Endogenous Endophthalmitis in the Developing World
J. Arevalo (2010)
Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy.
S. Schröder (1991)
In vivo demonstration of increased leukocyte entrapment in retinal microcirculation of diabetic rats.
K. Miyamoto (1998)
Septic metastatic endophthalmitis complicating Klebsiella pneumoniae liver abscess in a non-diabetic Chinese man.
T. Y. Wong (2001)
Septic metastatic endophthalmitis complicating Klebsiella pneumoniae liver abscess in a non-diabetic Chinese man.
Wong Ty (2001)
10.1160/TH08-06-0395
Contribution of (sub)domains of Staphylococcus aureus fibronectin-binding protein to the proinflammatory and procoagulant response of human vascular endothelial cells.
Ruth Heying (2009)
10.1146/annurev.micro.112408.134309
Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus.
M. Otto (2010)
10.1111/j.1365-2958.1995.mmi_17061143.x
Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes.
C. Greene (1995)
10.1126/SCIENCE.285.5428.760
Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall.
S. Mazmanian (1999)
10.1086/520437
Community-acquired methicillin-resistant Staphylococcus aureus in hospitalized adults and children without known risk factors.
E. Gorak (1999)
ImageJ. Bethesda, MD: National Institutes of Health. 1997–2014
WS Rasband (2015)
10.1007/s001250100588
Constitutive nitric oxide synthase is associated with retinal vascular permeability in early diabetic rats
M. Takeda (2001)
10.1203/PDR.0b013e31819dc44d
Molecular Pathogenesis of Staphylococcus aureus Infection
G. Y. Liu (2009)
10.1016/j.survophthal.2014.06.002
Systematic review of 342 cases of endogenous bacterial endophthalmitis.
T. Jackson (2014)
Methicillin-resistant Staphylococcus aureus infections of the eye and orbit (an American Ophthalmological Society thesis).
P. Blomquist (2006)
10.1089/10445490260099683
Host-parasite interactions in Staphylococcus aureus keratitis.
B. Jett (2002)
10.1007/S00268-003-6963-2
Ocular Manifestations and Complications of Pyogenic Liver Abscess
Yu-meng Tan (2004)
10.1128/IAI.66.8.4004-4007.1998
Synthesis of Microcapsule by Staphylococcus aureus Is Not Responsive to Environmental Phosphate Concentrations
K. Fox (1998)
10.1016/J.JHIN.2004.07.014
Epidemiology of capsular and surface polysaccharide in Staphylococcus aureus infections complicated by bacteraemia.
M. Roghmann (2005)
10.1167/iovs.08-2085
A role for tumor necrosis factor-alpha in experimental Bacillus cereus endophthalmitis pathogenesis.
R. T. Ramadan (2008)
10.1128/IAI.68.6.3776-3779.2000
The Collagen-Binding Adhesin Is a Virulence Factor in Staphylococcus aureus Keratitis
M. Rhem (2000)
10.1128/IAI.66.11.5183-5189.1998
Staphylococcus aureus Serotype 5 Capsular Polysaccharide Is Antiphagocytic and Enhances Bacterial Virulence in a Murine Bacteremia Model
M. Thakker (1998)
10.1128/IAI.01330-07
Bacillus cereus Induces Permeability of an In Vitro Blood-Retina Barrier
A. L. Moyer (2008)
10.1016/S0039-6257(03)00054-7
Endogenous bacterial endophthalmitis: a 17-year prospective series and review of 267 reported cases.
T. Jackson (2003)
10.2337/diacare.18.9.1314
American Diabetes Association Scientific Sessions, 1995: Neuropathy and Retinopathy
Z. Bloomgarden (1995)
10.1128/IAI.70.7.3389-3395.2002
Overproduction of Type 8 Capsular Polysaccharide Augments Staphylococcus aureus Virulence
T. Luong (2002)
10.1002/(SICI)1097-4547(19970801)49:3<268::AID-JNR2>3.0.CO;2-A
Blood-retinal barrier (BRB) breakdown in experimental autoimmune uveoretinitis: comparison with vascular endothelial growth factor, tumor necrosis factor alpha, and interleukin-1beta-mediated breakdown.
J. Luna (1997)
10.1099/mic.0.032466-0
Transcription of the phage-encoded Panton-Valentine leukocidin of Staphylococcus aureus is dependent on the phage life-cycle and on the host background.
C. Wirtz (2009)
10.1167/IOVS.04-0247
Death of retinal neurons in streptozotocin-induced diabetic mice.
P. Martin (2004)



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10.1136/bcr-2017-219296
Endogenous endophthalmitis and osteomyelitis associated with interleukin 17 inhibitor treatment for psoriasis in a patient with diabetes
C. E. Martinez (2017)
10.3390/pathogens7010009
The Pathogenesis of Staphylococcus aureus Eye Infections
Richard J O'Callaghan (2018)
10.1128/mSphere.00262-19
Disarming Pore-Forming Toxins with Biomimetic Nanosponges in Intraocular Infections
P. Coburn (2019)
10.1371/journal.pone.0154560
Bloodstream-To-Eye Infections Are Facilitated by Outer Blood-Retinal Barrier Dysfunction
P. Coburn (2016)
10.1371/journal.pone.0227121
Detection of Torque Teno Virus (TTV) and TTV-Like Minivirus in patients with presumed infectious endophthalmitis in India
Poonam Naik (2020)
10.1007/s00430-019-00627-4
Interplay between IDO1 and iNOS in human retinal pigment epithelial cells
Katrin Spekker-Bosker (2019)
10.1101/2020.07.06.190264
Immune Inhibitor A Metalloproteases Contribute to Virulence in Bacillus Endophthalmitis
E. Livingston (2020)
10.1016/j.preteyeres.2016.04.007
Modeling intraocular bacterial infections
R. Astley (2016)
10.1136/bcr-2018-227025
Endogenous bacterial endophthalmitis and subretinal abscess complicating diabetic ketoacidosis
J. P. Harvey (2018)
10.1080/09273948.2017.1355469
Culture-Positive Endogenous Endophthalmitis: An Eleven-Year Retrospective Study in the Central Region of Thailand
Sukhum Silpa-archa (2018)
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