Heparan sulfate proteoglycans mediate Staphylococcus aureus interactions with intestinal epithelium

Medical Microbiology and Immunology

Volumn 195, Issue 3, 2006, Pages 133-141

  Hess, Donavon J ^a   Henry Stanley, Michelle J ^b   Erlandsen, Stanley L ^b   Wells, Carol L ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Enterocyte; Fibronectin; Heparan sulfate; Staphylococcus aureus

Indexed keywords

FIBRONECTIN BINDING PROTEIN; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIUM ADHERENCE; CELL CULTURE; CELL LINE; CELL SURFACE; CELL TRANSPORT; CHO CELL; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL ADHESION; CACO-2 CELLS; CHO CELLS; CRICETINAE; CRICETULUS; EPITHELIAL CELLS; HEPARITIN SULFATE; HUMANS; INTESTINES; PROTEOGLYCANS; RECEPTORS, CELL SURFACE; STAPHYLOCOCCUS AUREUS; SYNDECAN-1;

EID: 33748857194     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00430-005-0007-5     Document Type: Article

References (47)

1. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, Hook M (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMS and host cell β1 integrins. Eur J Cell Biol 79:672-679
2. Gresham HD, Lowrance JH, Caver TE, Wilson BS, Cheung AL, Lindberg FP (2000) Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol 164:3717-3722
3. Kahl BC, Goulian M, Wamel Wv, Herrmann M, Simon SM, Kaplan G, Peters G, Cheung AL (2000) Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect Immun 68:5385-5392
4. Kintarak S, Whawell S, Speight P, Packer S, Nair S (2004) Internalization of Staphylococcus aureus by human keratinocytes. Infect Immun 72:5668-5675
5. Jett B, Gilmore M (2002) Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectin-binding protein and host cell factors. Infect Immun 70:4697-4700
6. Finegold SM, Mathisen GE, George WL (1983) Changes in human intestinal flora related to the administration of antimicrobial agents. In: Hentges DJ (ed) Human intestinal microflora in health and disease. Academic, New York, pp 355-446
7. Clark NM, Hershberger E, Zervosc MJ, Lynch JP (2003) Antimicrobial resistance among gram-positive organisms in the intensive care unit. Curr Opin Crit Care 9:403-412
8. Greene C, McDevitt D, Francois P, Vaudaux PE, Lew DP, Foster TJ (1995) Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol Microbiol 17:1143-1152
9. Sinha B, Francois P, Que Y-A, Hussain M, Heilmann C, Moreillon P, Lew D, Krause K-H, Peters G, Herrmann M (2000) Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 68:6871-6878
10. Ahmed S, Meghji S, Williams R, Henderson B, Brock J, Nair S (2001) Staphylococcus aureus fibronectin binding proteins are essential for internalization by osteoblasts but do not account for differences in intracellular levels of bacteria. Infect Immun 69:2872-2877
11. Brouillette E, Grondin G, Shkreta L, Lacasse P, Talbot B (2003) In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin binding proteins. Microb Pathog 35:159-168
12. Mongodin E, Bajolet O, Cutrona J, Bonnet N, Dupuit F, Puchelle E, Bentzmann S (2002) Fibronectin-binding proteins of Staphylococcus aureus are involved in adherence to human airway epithelium. Infect Immun 70:620-630
13. Duensing TD, Wing JS, van Putten JPM (1999) Sulfated polysaccharide- directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect Immun 67:4463-4468
14. Fleckstein JM, Holland JT, Hasty DL (2002) Interaction of an outer membrane protein of enterotoxigenic Escherichia coli with cell surface heparan sulfate proteoglycans. Infect Immun 70:1530-1537
15. Rostand KS, Esko JD (1997) Microbial adherence to and invasion through proteoglycans. Infect Immun 65:1-8
16. Esko JD, Lindahl U (2001) Molecular diversity of heparan sulfate. J Clin Invest 108:169-173
17. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Ann Rev Biochem 68:729-777
18. Liang OD, Ascencio F, Fransson LA, Wadstrom T (1992) Binding of heparan sulfate to Staphylococcus aureus. Infect Immun 60:899-906
19. Henry-Stanley MJ, Hess DJ, Erickson EA, Garni RM, Wells CL (2003) Role of heparan sulfate in interaction of Listeria monocytogenes with enterocytes. Med Microbiol Immunol 192:107-115
20. Menzies BE, Kourteva I (1998) Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun 66:5994-5998
21. Hidalgo I, Raub T, Borchardt R (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial cell permeability. Gastroenterology 96:736-749
22. Neutra M, Louvard D (1989) Differentiation of intestinal epithelial cells in vitro. In: Satir BH (ed) Functional epithelial cells in culture. AR Liss, New York, pp 363-98
23. Pinto M, Robine-Leon S, Apay M, Kedinger M, Triadou N, Dussaulx E, Lacroix B, Simon-Assman P, Haffen K, Fogh J, Zweibaum A (1983) Enterocyte-like differentiation and polarization of the human colon cancer cell line Caco-2 in culture. Biol Cell 47:3223-3228
24. Wells CL, Jechorek RP, Olmsted SB, Erlandsen SL (1994) Bacterial translocation in cultured enterocytes: magnitude, specificity, and electron microscopic observations of endocytosis. Shock 1:1443-1451
25. Wells CL, van de Westerlo EMA, Jechorek RP, Erlandsen SL (1998) Cytochalasin-induced actin disruption of polarized enterocytes can augment internalization of bacteria. Infect Immun 66:2410-2419
26. Wells CL, van de Westerlo EMA, Jechorek RP, Feltis BA, Wilkins TD, Erlandsen SL (1996) Bacteroides fragilis enterotoxin modulates epithelial permeability and bacterial internalization by HT-29 enterocytes. Gastroenterol 110:1429-1437
27. Wells CL, van de Westerlo EMA, Jechorek RP, Erlandsen SL (1995) Exposure of the lateral enterocyte membrane by dissociation of calcium-dependent junctional complex augments endocytosis of enteric bacteria. Shock 4:204-210
28. Day R, Ilyas M, Daszak P, Talbot I, Forbes A (1999) Expression of syndecan-1 in inflammatory bowel disease and a possible mechanism of heparin therapy. Dig Dis Sci 44:2508-2515
29. Hess DJ, Henry-Stanley MJ, Moore EA, Wells CL (2001) Integrin expression, enterocyte maturation, and bacterial internalization. J Surg Res 98:116-122
30. Kjellen L, Lindahl U (1991) Proteoglycans: structures and interactions. Ann Rev Biochem 60:443-475
31. Stanley MJ, Liebersbach BF, Liu W, Anhalt DJ, Sanderson RD (1995) Heparan sulfate-mediated cell aggregation: syndecans-1 and -4 mediate intercellular adhesion following their transfection into human B lymphoid cells. J Biol Chem 270:5077-5083
32. Lidholt K, Weinke JL, Kiser CS, Lugemwa FN, Bame KJ, Cheifetz S, Massague J, Lindahl U, Esko JD (1992) A single mutation affects both N-acetylglucosamine/transferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc Natl Acad Sci USA 89:2267-2271
33. Esko JD, Stewart TE, Taylor WH (1985) Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci USA 82:3197-3201
34. Liebersbach BF, Sanderson RD (1994) Expression of syndecan-1 inhibits cell invasion into type I collagen. J Biol Chem 269:20013-20019
35. Vaudaux P, Avramoglou T, Letourneur D, Lew DP, Jozefonvicz J (1992) Inhibition by heparin and derivatized dextrans of Staphylococcus aureus adhesion to fibronectin-coated biomaterials. J Biomat Sci Polym Ed 4:89-97
36. Rimland D, Roberson B (1986) Gastrointestinal carriage of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 24:137-138
37. Hess DJ, Henry-Stanley MJ, Erickson EA, Wells CL (2003) Intracellular survival of Staphylococcus aureus within cultured enterocytes. J Surg Res 114:42-49
38. Liang OD, Flock JI, Wadstrom T (1995) Isolation and characterization of a vitronectin-binding surface protein from Staphylococcus aureus. Biochim Biophys Acta 1250:110-116
39. Kazmierczak BI, Mostov K, Engel JN (2001) Interaction of bacterial pathogens with polarized epithelium. Ann Rev Microbiol 55:407-435
40. Wells CL, Moore EA, Hoag JA, Hirt H, Dunny GM, Erlandsen SL (2000) Inducible expression of Enterococcus faecalis aggregation substance surface protein facilitates bacterial internalization of cultured enterocytes. Infect Immun 68:7190-7194
41. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trelstad RL, Bernfield M (1987) Immunohistochemistry of cell surface heparan sulfate proteoglycan in mouse tissues: a light and electron microscopic study. J Histochem Cytochem 35:1079-1088
42. De-Souza DA, Greene LJ (2005) Intestinal permeability and systemic infections in critically ill patients: effect of glutamine. Crit Care Med 33:1125-1135
43. Laupland KB, Kirkpatrick AW, Church DL, Ross T, Gregson DB (2004) Intensive-care-unit-acquired bloodstream infections in a regional critically ill population. J Hosp Infect 58:137-145
44. Clarke SR, Harris LG, Richards RG, Foster SJ (2002) Analysis of Ebh, a 1.1 megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect Immun 70:6680-6687
45. Harraghy N, Hussain M, Haggar A, Chavakis T, Sinha B, Herrmann M, Flock J-I (2003) The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiol 149:2701-2707
46. + gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin, and integrin receptors. Mol Microbiol 29:369-379
47. Dziewanowska K, Carson A, Patti J, Deobald C, Bayles K, Bohach G (2000) Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells. Infect Immun 68:6321-6328