Blood–retinal barrier compromise and endogenous Staphylococcus aureus endophthalmitis

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 12, 2015, Pages 7303-7311

  Coburn, Phillip S ^a   Wiskur, Brandt J ^b   Astley, Roger A ^a   Callegan, Michelle C ^a,b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

Bacteria; Blood retinal barrier; Diabetes; Endogenous endophthalmitis; Retinal pigment epithelium; Staphylococcus aureus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BLOOD RETINA BARRIER; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE DURATION; ELECTRORETINOGRAPHY; ENDOPHTHALMITIS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; KLEBSIELLA PNEUMONIAE; MALE; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; BACTERIAL EYE INFECTION; C57BL MOUSE; DISEASE MODEL; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

ANIMALS; BLOOD-RETINAL BARRIER; DISEASE MODELS, ANIMAL; ENDOPHTHALMITIS; EYE INFECTIONS, BACTERIAL; MALE; MICE; MICE, INBRED C57BL; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84946924771     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-17488     Document Type: Article

References (64)

1. Jackson TL, Paraskevopoulos T, Georgalas I. Systematic review of 342 cases of endogenous bacterial endophthalmitis. Surv Ophthalmol. 2014;59:627-635.
2. Ho V, Ho LY, Ranchod TM, Drenser KA, Williams GA, Garretson BR. Endogenous methicillin-resistant Staphylococcus aureus endophthalmitis. Retina. 2011;31:596-601.
3. Durand ML. Endophthalmitis. Clin Microbiol Infect. 2013;19: 227-234.
4. Arevalo J, Jap A, Chee S, Zeballos D. Endogenous endophthalmitis in the developing world. Int Ophthalmol Clin. 2010;50: 173-187.
5. Greenwald MJ, Wohl LG, Sell CH. Metastatic bacterial endophthalmitis: a contemporary reappraisal. Surv Ophthalmol. 1986;31:81-101.
6. Jackson TL, Eykyn SJ, Graham EM, Stanford MR. Endogenous bacterial endophthalmitis: a 17-year prospective series and review of 267 reported cases. Surv Ophthalmol. 2003;48:403- 423.
7. Okada AA, Johnson RP, Liles WC, D'Amico DJ, Baker AS. Endogenous bacterial endophthalmitis: report of a ten-year retrospective study. Ophthalmology. 1994;101:832-838.
8. Liu GY. Molecular pathogenesis of Staphylococcus aureus infection. Pediatr Res. 2009;65:71R-77R.
9. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339:520-532.
10. Major JC Jr, Engelbert M, Flynn HW Jr, Miller D, Smiddy WE, Davis JL. Staphylococcus aureus endophthalmitis: antibiotic susceptibilities, methicillin resistance, and clinical outcomes. Am J Ophthalmol. 2010;149:278-283.
11. Ness T, Schneider C. Endogenous endophthalmitis caused by methicillin-resistant Staphylococcus aureus (MRSA). Retina. 2009;29:831-834.
12. Nixdorff NA, Tang J, Mourad R, Skalweit MJ. SAME is different: a case report and literature review of Staphylococcus aureus metastatic endophthalmitis. South Med J. 2009;102:952-956.
13. Gorak EJ, Yamada SM, Brown JD. Community-acquired methicillin-resistant Staphylococcus aureus in hospitalized adults and children without known risk factors. Clin Infect Dis. 1999;29:797-800.
14. Blomquist PH. Methicillin-resistant Staphylococcus aureus infections of the eye and orbit [American Ophthalmological Society thesis]. Trans Am Ophthalmol Soc. 2006;104:322- 345.
15. Wong TY, Chiu SI, So MK, et al. Septic metastatic endophthalmitis complicating Klebsiella pneumoniae liver abscess in a non-diabetic Chinese man. Hong Kong Med J. 2001;7:303- 306.
16. Tan YM, Chee SP, Soo KC, Chow P. Ocular manifestations and complications of pyogenic liver abscess. World J Surg. 2004; 28:38-42.
17. Coburn PS, Wiskur BJ, Christy E, Callegan MC. The diabetic ocular environment facilitates the development of endogenous bacterial endophthalmitis. Invest Ophthalmol Vis Sci. 2012; 53:7426-7431.
18. Jo DH, Kim JH, Kim JH. How to overcome retinal neuropathy: the fight against angiogenesis-related blindness. Arch Pharm Res. 2010;33:1557-1565.
19. Schroder S, Palinski W, Schmid-Schonbein GW. Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am J Pathol. 1991;139:81-100.
20. Miyamoto K, Hiroshiba N, Tsujikawa A, Ogura Y. In vivo demonstration of increased leukocyte entrapment in retinal microcirculation of diabetic rats. Invest Ophthalmol Vis Sci. 1998;39:2190-2194.
21. Miyamoto K, Khosrof S, Bursell SE, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A. 1999;96:10836-10841.
22. Funatsu H, Yamashita H, Sakata K, et al. Vitreous levels of vascular endothelial growth factor and intercellular adhesion molecule 1 are related to diabetic macular edema. Ophthalmology. 2005;112:806-816.
23. Fong DS, Aiello L, Gardner TW, et al. American Diabetes Association: diabetic retinopathy. Diabetes Care. 2003;26: 226-229.
24. Neely KA, Gardner TW. Ocular neovascularization: clarifying complex interactions. Am J Pathol. 1998;153:665-670.
25. Qaum T, Xu Q, Joussen AM, et al. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest Ophthalmol Vis Sci. 2001;42:2408-2413.
26. Takeda M, Mori F, Yoshida A, et al. Constitutive nitric oxide synthase is associated with retinal vascular permeability in early diabetic rats. Diabetologia. 2001;44:1043-1050.
27. Asnaghi V, Gerhardinger C, Hoehn T, Adeboje A, Lorenzi M. A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes. 2003;52:506-511.
28. Martin PM, Roon P, Van Ells TK, Ganapathy V, Smith SB. Death of retinal neurons in streptozotocin induced diabetic mice. Invest Ophthalmol Vis Sci. 2004;45:3330-3336.
29. Novick R. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology. 1967;33:155-166.
30. Booth M, Atkuri R, Nanda S, Iandolo J, Gilmore M. Accessory gene regulator controls Staphylococcus aureus virulence in endophthalmitis. Invest Ophthalmol Vis Sci. 1995;36:1828- 1836.
31. Callegan M, Booth M, Jett B, Gilmore M. Pathogenesis of grampositive bacterial endophthalmitis. Infect Immun. 1999;67: 3348-3356.
32. Engelbert M, Gilmore M. Fas ligand but not complement is critical for control of experimental Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci. 2005;46:2479- 2486.
33. Ramadan RT, Ramirez R, Novosad BD, Callegan MC. Acute inflammation and loss of retinal architecture and function during experimental Bacillus endophthalmitis. Curr Eye Res. 2006;31:955-965.
34. Ramadan RT, Moyer AL, Callegan MC. A role for tumor necrosis factor-alpha in experimental Bacillus cereus endophthalmitis pathogenesis. Invest Ophthalmol Vis Sci. 2008;49: 4482-4489.
35. Moyer AL, Ramadan RT, Thurman J, Burroughs A, Callegan MC. Bacillus cereus induces permeability of an in vitro bloodretina barrier. Infect Immun. 2008;76:1358-1367.
36. Rasband WS. ImageJ. Bethesda, MD: National Institutes of Health. 1997-2014. Available at: http://imagej.nih.gov/ij/. Accessed April 30, 2015.
37. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671-675.
38. Abramoff MD, Magalhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11:36-42.
39. Wiskur BJ, Hunt JJ, Callegan MC. Hypermucoviscosity as a virulence factor in experimental Klebsiella pneumoniae endophthalmitis. Invest Ophthalmol Vis Sci. 2008;49:4931- 4938.
40. Hunt JJ, Wang JT, Callegan MC. Contribution of mucoviscosity associated gene A (magA) to virulence in experimental Klebsiella pneumoniae endophthalmitis. Invest Ophthalmol Vis Sci. 2011;52:6860-6866.
41. Mazmanian SK, Liu G, Ton-That H, Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science. 1999;285:760-763.
42. Navarre WW, Schneewind O. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram positive bacteria. Mol Microbiol. 1994;14:115-121.
43. Greene C, McDevitt D, François P, Vaudaux P, Lew D, Foster T. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin binding proteins and studies on the expression of the fnb genes. Mol Microbiol. 1995;17:1143- 1152.
44. McDevitt D, François P, Vaudaux P, Foster T. Molecular characterization of the fibrinogen receptor (clumping factor) of Staphylococcus aureus. Mol Microbiol. 1994;11:237-248.
45. Patti J, Jonsson H, Guss B, et al. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesion. J Biol Chem. 1992;267:4766-4772.
46. Jett BD, Gilmore MS. Host-parasite interactions in Staphylococcus aureus keratitis. DNA Cell Biol. 2002;21:397-404.
47. Jett BD, Gilmore MS. Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectinbinding protein and host cell factors. Infect Immun. 2002;70: 4697-4700.
48. Rhem MN, Lech EM, Patti JM, et al. The collagen-binding adhesin is a virulence factor in Staphylococcus aureus keratitis. Infect Immun. 2000;68:3776-3779.
49. Mattsson E, Heying R, van de Gevel JS, Hartung T, Beekhuizen H. Staphylococcal peptidoglycan initiates an inflammatory response and procoagulant activity in human vascular endothelial cells: a comparison with highly purified lipoteichoic acid and TSST-1. FEMS Immunol Med Microbiol. 2008;52:110-117.
50. Heying R, van de Gevel J, Que YA, Piroth L, Moreillon P, Beekhuizen H. Contribution of (sub)domains of Staphylococcus aureus fibronectin-binding protein to the proinflammatory and procoagulant response of human vascular endothelial cells. Thromb Haemost. 2009;101:495-504.
51. Kerdudou S, Laschke MW, Sinha B, Preissner KT, Menger MD, Herrmann M. Fibronectin binding proteins contribute to the adherence of Staphylococcus aureus to intact endothelium in vivo. Thromb Haemost. 2006;96:183-189.
52. Edwards AM, Bowden MG, Brown EL, Laabei M, Massey RC. Staphylococcus aureus extracellular adherence protein triggers TNFα release, promoting attachment to endothelial cells via protein A. PLoS One. 2012;7:e43046.
53. Wang JE, Jørgensen PF, Almlöf M, et al. 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. Infect Immun. 2000;68:3965-3970.
54. Luna JD, Chan CC, Derevjanik NL, et al. 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 Neurosci Res. 1997;49:268-280.
55. Herbert S, Ziebandt AK, Ohlsen K, et al. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun. 2010;78: 2877-2889.
56. Plata K, Rosato A, Wegrzyn G. Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity. Acta Biochim Pol. 2009;56:597- 612.
57. Wirtz C, Witte W, Wolz C, Goerke C. Transcription of the phage-encoded Panton-Valentine leukocidin of Staphylococcus aureus is dependent on the phage life-cycle and on the host background. Microbiology. 2009;155:3491-3499.
58. Otto M. Basis of virulence in community-associated methicillin- resistant Staphylococcus aureus. Annu Rev Microbiol. 2010;64:143-162.
59. Löffler B, Hussain M, Grundmeier M, et al. Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 2010;6:e1000715.
60. Ibberson CB, Jones CL, Singh S, et al. Staphylococcus aureus hyaluronidase is a CodY-regulated virulence factor. Infect Immun. 2014;82:4253-4264.
61. Luong T, Lee C. Overproduction of type 8 capsular polysaccharide augments Staphylococcus aureus virulence. Infect Immun. 2002;70:3389-3395.
62. Thakker M, Park J, Carey V, Lee J. Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun. 1998;66:5183-5189.
63. Roghmann M, Taylor K, Gupte A, et al. Epidemiology of capsular and surface polysaccharide in Staphylococcus aureus infections complicated by bacteraemia. J Hosp Infect. 2005;59: 27-32.
64. Fox KF, Stewart GC, Fox A. Synthesis of microcapsule by Staphylococcus aureus is not responsive to environmental phosphate concentrations. Infect Immun. 1998;66:4004- 4007.