Role of heparan sulfate in interactions of Listeria monocytogenes with enterocytes

Medical Microbiology and Immunology

Volumn 192, Issue 2, 2003, Pages 107-115

  Henry Stanley, Michelle J ^a   Hess, Donavon J ^a   Erickson, Elizabeth A ^a   Garni, Robb M ^a   Wells, Carol L ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Enterocyte; Heparan sulfate; Heparin; Listeria monocytogenes; Syndecan 1

Indexed keywords

CHONDROITIN SULFATE; COMPLEMENTARY DNA; CORE PROTEIN; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; HEPARIN BINDING PROTEIN; HYALURONIC ACID; SYNDECAN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIUM ADHERENCE; CELL STRAIN HT29; COLON; CONTROLLED STUDY; FEMALE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTERNALIZATION; INTESTINE CELL; LISTERIA MONOCYTOGENES; LISTERIOSIS; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; SMALL INTESTINE;

EID: 0038130974     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00430-002-0165-7     Document Type: Article

References (47)

1. Alvarez-Dominguez C, Vazquez-Boland J.-A, Carrasco-Marin, E Lopez-Mato P, Leyva-Cobian F (1997) Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun 65:78-88
2. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ (1992) Biology of the syndecans: a family of transmembrane heparin sulfate proteoglycans. Annu Rev Cell Biol 8:365-393
3. Chen JC-R, Stephens RS (1977) Chlamydia trachomatis glycosaminoglycan-dependent and independent attachment to eukaryotic cells. Microb Pathog 2:23-30
4. Cossart P, Bierne H (2001) The use of host cell machinery in the pathogenesis of Listeria monocytogenes. Curr Opin Immunol 13:96-103
5. Couchman JR, Woods A (1996) Syndecans, signaling, and cell adhesion. J Cell Biochem 61:578-584
6. David G, Bai XM, Van der Schueren B, Cassiman JJ, Van den Berghe H (1992) Developmental changes in heparan sulfate expression: in situ detection with mAbs. J Cell Biol 119:961-975
7. 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
8. Day RM, Hao X, Ilyas M, Daszak P, Talbot IC, Forbes A (1999) Changes in the expression of syndecan-1 in the colorectal-adenoma-carcinoma sequence. Virchows Arch 434:121-125
9. Duensing TD, Wing JS, Putten JPM van (1999) Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect Immun 67:4463-4468
10. Esko JD, Lindahl U (2001) Molecular diversity of heparan sulfate. J Clin Invest 108:169-173
11. Finlay BB, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61:136-169
12. Goldberg MB (2001) Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 65:595-626
13. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trelstad RL, Bernfield M (1987) Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues: a light and electron microscopic study. J Histochem Cytochem 35:1079-1088
14. Huet C, Sahuquillo-Merino E, Courdrier E, Louvard D (1987) Absorptive and mucus-screening subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol 105:345-357
15. Jonquieres R, Pizarro-Cerda J, Cossart P (2001) Synergy between the N-and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes. Mol Microbiol 42:955-965
16. Kim CW, Goldberger OA, Gallo R L, Bernfield M (1994) Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns Mol Biol Cell 5:797-805
17. Kjellen L, Lindahl U (1991) Proteoglycans: structures and interactions. Annu Rev Biochem 60:443-475
18. Langford JK, Stanley M J, Cao D, Sanderson RD (1998) Multiple heparan sulfate chains are required for syndecan-1 function. J Biol Chem 273:29965-29971
19. Lecuit M, Dramsi S, Gottardi C, Fedor-Chaiken M, Gumbiner B, Cossart P (1999) A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes EMBO J 18:3956-3963
20. Leppa S, Vleminck K, Van Roy F, Jalkanen M (1996) Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin dependent. J Cell Science 109:1393-1403
21. Leroy A, Noe V, Mareel M, Neils H (1997) Glycoconjugate cross-talk in metastatic cancer cells, leucocytes, parasites and bacteria. Biochem Soc Trans 25:228-234
22. Levy P, Munier A, Baron-Delage S, DiGioia Y, Gespach C, Capeau C, Cherqui, G (1996) Syndecan-1 alterations during tumorgenic pregression of human colonic Caco-2 cells induced by human Ha-ras or polyoma middle T oncogenes. Br J Cancer 74:423-431
23. Liu W, Litwack ED, Stanley MJ, Langford JK, Lander AD, Sanderson RD (1998) Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J Biol Chem 273:22825-22832
24. Mengaud J, Ohanyon H, Gounon P, Mege R, Cossart P (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923-932
25. Mertens G, Van der Schueren B, Berghe H van den, David G (1996) Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J Cell Biol 132:487-497
26. Neutra M, Louvard D (1989) Differentiation of intestinal epithelial cells in vitro. In: Satir BH (ed) Functional epithelial cells in culture. Liss, New York, pp 363-398
27. Paulsson M, Gouda I, Larm O, Ljungh A (1994) Adherence of coagulase-negative staphylococci to heparin and other glycosaminoglycans immobilized on polymer surfaces. J Biomed Mater Res 28:311-317
28. Perrimin N, Bernfield M (2001) Cellular functions of proteoglycans - an overview. Semin Cell Dev Biol 12:65-67
29. Pethe K, Aumercier M, Fort E, Gatot C, Locht C, Menozzi FD (2000) Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin. J Biol Chem 275:14273-14280
30. Pinto M, Robine-Leon S, Apay M-D, 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 carcinoma cell line Caco-2 in culture. Biol Cell 47:323-330
31. Rapraeger AC (1993) The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr Biol 5:844-853
32. Rostand KS, Esko JD (1997) Microbial adherence to and invasion through proteoglycans. Infect Immun 65:1-8
33. Sawitzky D (1996) Protein-glycosaminoglycan interactions: infectiological aspects. Med Microbiol Immunol 184:155-161
34. 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
35. Stanley MJ, Stanley MW, Sanderson RD, Zera R (1999). Syndecan-1 expression is induced in the stroma of infiltrating breast carcinoma. Am J Clin Pathol 112:377-383
36. Suarez M, Gonzalez-Zorn B, Vega Y, Chico-Calero I, Vazquez-Boland J-A (2001) A role for ActA in epithelial cell invasion by Listeria monocytogenes Cell Microbiol 3:853-864
37. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, Goebel W, Gonzalez-Zorn B, Wehland J, Kreft J (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584-640
38. Wells CL, Erlandsen SL (1991) Localization of translocating Escherichia coli, Proteus mirabilis, and Enterococcus faecalis within cecal and colonic tissue of monoassociated mice. Infect Immun 59:4693-4697
39. Wells CL, Jechorek RP, Olmsted SB, Erlandsen SL (1994) Bacterial translocation in cultured enterocytes: magnitude, specificity, and electron microscopic observations of endocytosis. Shock 1:443-451
40. Wells CL, Westerlo EMA van de, 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
41. Wells CL, Westerlo EMA van de, Jechorek RP, Erlandsen SL (1996) Effect of hypoxia on enterocyte internalization of enteric bacteria. Crit Care Med 24:985-991
42. Wells CL, Westerlo EMA van de, Jechorek RP, Feltis BA, Wilkins TD, Erlandsen SL (1996) Bacteroides fragilis enterotoxin modulates epithelial permeability and bacterial internalization by HT-29 enterocytes. Gastroenterology 110:1429-1437
43. Wells CL, Westerlo EMA van de, Jechorek RP, Erlandsen, SL (1998) Cytochalasin-induced actin disruption of polarized enterocytes can augment internalization of bacteria. Infect Immun 66:2410-2419
44. Wells CL, Jechorek RP, Kinneberg KM, Debol SM, Erlandsen SL (1999) The isoflavone genistein inhibits internalization of enteric bacteria by cultured Caco-2 and HT-29 enterocytes. J Nutr 129:634-640
45. 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
46. Westphal V, Murch, S, Kim S, Srikrishna G, Winchester B, Day R, Freeze H (2000) Reduced heparan sulfate accumulation in enterocytes contributes in protein-losing enteropathy in a congenital disorder of glycosylation. Am J Pathol 157:1917-1925
47. Wijdenes J, Vooijs W, Clement C, Post J, Morad F, Vita N, Laurent P, Sun R, Klein B, Bore J (1996) A plasmocyte selective monoclonal antibody (B-B4) recognizes syndecan-1. Br J Haematol 94:318-323