Glycosaminoglycan binding facilitates entry of a bacterial pathogen into central nervous systems

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Chang, Yung Chi ^a,b   Wang, Zhipeng ^c,d   Flax, Lindsay A ^c   Xu, Ding ^a,e   Esko, Jeffrey D ^a,e   Nizet, Victor ^a,b,f,g   Baron, Miriam J ^c,h  

^a University of California San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g RADY CHILDREN'S HOSPITAL   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GLYCOSAMINOGLYCAN; ALPHA C PROTEIN, GROUP B STREPTOCOCCI; BACTERIAL PROTEIN; MEMBRANE ANTIGEN;

ARTICLE; BACTERIAL MENINGITIS; BACTERIAL VIRULENCE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; GROUP B STREPTOCOCCAL INFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PATHOGENESIS; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS AGALACTIAE; ANIMAL; BACTERIAL INFECTION; BRAIN; ENDOTHELIUM CELL; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PATHOLOGY; PROTEIN BINDING; VASCULAR ENDOTHELIUM;

BACTERIA (MICROORGANISMS); HEXAPODA; MAMMALIA; MUS; STREPTOCOCCUS SP. 'GROUP B';

ANIMALS; ANTIGENS, SURFACE; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; BLOOD-BRAIN BARRIER; BRAIN; CENTRAL NERVOUS SYSTEM; DROSOPHILA; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GLYCOSAMINOGLYCANS; HUMANS; MICE; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; STREPTOCOCCUS AGALACTIAE;

EID: 79959855148     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002082     Document Type: Article

References (66)

1. Organization WH, (2004) The World Health Report 2004: changing history.
2. Edwards MS, Rench MA, Haffar AA, Murphy MA, Desmond MM, et al. (1985) Long-term sequelae of group B streptococcal meningitis in infants. J Pediatr 106: 717-722.
3. Stevens JP, Eames M, Kent A, Halket S, Holt D, et al. (2003) Long term outcome of neonatal meningitis. Arch Dis Child Fetal Neonatal Ed 88: F179-184.
4. Galiza EP, Heath PT, (2009) Improving the outcome of neonatal meningitis. Curr Opin Infect Dis 22: 229-234.
5. Berardi A, Lugli L, Rossi C, China MC, Vellani G, et al. (2010) Neonatal bacterial meningitis. Minerva Pediatr 62: 51-54.
6. Schwartz B, Schuchat A, Oxtoby MJ, Cochi SL, Hightower A, et al. (1991) Invasive group B streptococcal disease in adults. A population-based study in metropolitan Atlanta. JAMA 266: 1112-1114.
7. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH, et al. (2008) Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 299: 2056-2065.
8. Skoff TH, Farley MM, Petit S, Craig AS, Schaffner W, et al. (2009) Increasing burden of invasive group B streptococcal disease in nonpregnant adults, 1990-2007. Clin Infect Dis 49: 85-92.
9. Kim KS, (2008) Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol 6: 625-634.
10. Maisey HC, Doran KS, Nizet V, (2008) Recent advances in understanding the molecular basis of group B Streptococcus virulence. Expert Rev Mol Med 10: e27.
11. Bishop JR, Schuksz M, Esko JD, (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030-1037.
12. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, et al. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68: 729-777.
13. Esko JD, Lindahl U, (2001) Molecular diversity of heparan sulfate. J Clin Invest 108: 169-173.
14. Rostand KS, Esko JD, (1997) Microbial adherence to and invasion through proteoglycans. Infect Immun 65: 1-8.
15. Bulow HE, Hobert O, (2006) The molecular diversity of glycosaminoglycans shapes animal development. Annu Rev Cell Dev Biol 22: 375-407.
16. Esko JD, Selleck SB, (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71: 435-471.
17. Lawrence R, Olson SK, Steele RE, Wang L, Warrior R, et al. (2008) Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling. J Biol Chem 283: 33674-33684.
18. Nakato H, Kimata K, (2002) Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim Biophys Acta 1573: 312-318.
19. Nybakken K, Perrimon N, (2002) Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila. Biochim Biophys Acta 1573: 280-291.
20. Shieh MT, WuDunn D, Montgomery RI, Esko JD, Spear PG, (1992) Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol 116: 1273-1281.
21. WuDunn D, Spear PG, (1989) Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 63: 52-58.
22. Pethe K, Alonso S, Biet F, Delogu G, Brennan MJ, et al. (2001) The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412: 190-194.
23. Alvarez-Dominguez C, Vazquez-Boland JA, 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.
24. Bolduc GR, Baron MJ, Gravekamp C, Lachenauer CS, Madoff LC, (2002) The alpha C protein mediates internalization of group B Streptococcus within human cervical epithelial cells. Cell Microbiol 4: 751-758.
25. Baron MJ, Bolduc GR, Goldberg MB, Auperin TC, Madoff LC, (2004) Alpha C protein of group B Streptococcus binds host cell surface glycosaminoglycan and enters cells by an actin-dependent mechanism. J Biol Chem 279: 24714-24723.
26. Baron MJ, Filman DJ, Prophete GA, Hogle JM, Madoff LC, (2007) Identification of a glycosaminoglycan binding region of the alpha C protein that mediates entry of group B streptococci into host cells. J Biol Chem 282: 10526-10536.
27. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, et al. (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123: 335-346.
28. Ayres JS, Freitag N, Schneider DS, (2008) Identification of Drosophila mutants altering defense of and endurance to Listeria monocytogenes infection. Genetics 178: 1807-1815.
29. Stoltz DA, Ozer EA, Taft PJ, Barry M, Liu L, et al. (2008) Drosophila are protected from Pseudomonas aeruginosa lethality by transgenic expression of paraoxonase-1. J Clin Invest 118: 3123-3131.
30. Sibley CD, Duan K, Fischer C, Parkins MD, Storey DG, et al. (2008) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.
31. Baron MJ, Wong SL, Nybakken K, Carey VJ, Madoff LC, (2009) Host glycosaminoglycan confers susceptibility to bacterial infection in Drosophila melanogaster. Infect Immun 77: 860-866.
32. Parker RJ, Auld VJ, (2006) Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17: 66-77.
33. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, et al. (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28: 587-597.
34. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, et al. (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29: 3538-3550.
35. Edwards TN, Meinertzhagen IA, (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90: 471-497.
36. Izumikawa T, Egusa N, Taniguchi F, Sugahara K, Kitagawa H, (2006) Heparan sulfate polymerization in Drosophila. J Biol Chem 281: 1929-1934.
37. Takei Y, Ozawa Y, Sato M, Watanabe A, Tabata T, (2004) Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 131: 73-82.
38. Toyoda H, Kinoshita-Toyoda A, Fox B, Selleck SB, (2000) Structural analysis of glycosaminoglycans in animals bearing mutations in sugarless, sulfateless, and tout-velu. Drosophila homologues of vertebrate genes encoding glycosaminoglycan biosynthetic enzymes. J Biol Chem 275: 21856-21861.
39. Kim KS, (2006) Microbial translocation of the blood-brain barrier. Int J Parasitol 36: 607-614.
40. Bobardt MD, Salmon P, Wang L, Esko JD, Gabuzda D, et al. (2004) Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J Virol 78: 6567-6584.
41. Floris S, van den Born J, van der Pol SM, Dijkstra CD, De Vries HE, (2003) Heparan sulfate proteoglycans modulate monocyte migration across cerebral endothelium. J Neuropathol Exp Neurol 62: 780-790.
42. Kim CW, Goldberger OA, Gallo RL, 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.
43. Leong JM, Wang H, Magoun L, Field JA, Morrissey PE, et al. (1998) Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells. Infect Immun 66: 994-999.
44. Stickens D, Zak BM, Rougier N, Esko JD, Werb Z, (2005) Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132: 5055-5068.
45. Tenenbaum T, Spellerberg B, Adam R, Vogel M, Kim KS, et al. (2007) Streptococcus agalactiae invasion of human brain microvascular endothelial cells is promoted by the laminin-binding protein Lmb. Microbes Infect 9: 714-720.
46. Maisey HC, Hensler M, Nizet V, Doran KS, (2007) Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 189: 1464-1467.
47. Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, et al. (2005) Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115: 2499-2507.
48. van Sorge NM, Quach D, Gurney MA, Sullam PM, Nizet V, et al. (2009) The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J Infect Dis 199: 1479-1487.
49. Doran KS, Liu GY, Nizet V, (2003) Group B streptococcal β-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J Clin Invest 112: 736-744.
50. McCormick C, Duncan G, Goutsos KT, Tufaro F, (2000) The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc Natl Acad Sci U S A 97: 668-673.
51. Senay C, Lind T, Muguruma K, Tone Y, Kitagawa H, et al. (2000) The EXT1/EXT2 tumor suppressors: catalytic activities and role in heparan sulfate biosynthesis. EMBO Rep 1: 282-286.
52. Kamimura K, Koyama T, Habuchi H, Ueda R, Masu M, et al. (2006) Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J Cell Biol 174: 773-778.
53. Kamimura K, Rhodes JM, Ueda R, McNeely M, Shukla D, et al. (2004) Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J Cell Biol 166: 1069-1079.
54. Stanford KI, Wang L, Castagnola J, Song D, Bishop JR, et al. (2010) Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem 285: 286-294.
55. Sugaya N, Habuchi H, Nagai N, Ashikari-Hada S, Kimata K, (2008) 6-O-sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J Biol Chem 283: 10366-10376.
56. Tonnaer EL, Hafmans TG, Van Kuppevelt TH, Sanders EA, Verweij PE, et al. (2006) Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect 8: 316-322.
57. de Vries FP, Cole R, Dankert J, Frosch M, van Putten JP, (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
58. Behling-Kelly E, Vonderheid H, Kim KS, Corbeil LB, Czuprynski CJ, (2006) Roles of cellular activation and sulfated glycans in Haemophilus somnus adherence to bovine brain microvascular endothelial cells. Infect Immun 74: 5311-5318.
59. Menozzi FD, Bischoff R, Fort E, Brennan MJ, Locht C, (1998) Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci U S A 95: 12625-12630.
60. Portugal MI, Todeschini AR, de Lima CS, Silva CA, Mohana-Borges R, et al. (2008) Characterization of two heparan sulphate-binding sites in the mycobacterial adhesin Hlp. BMC Microbiol 8: 75.
61. Capila I, Linhardt RJ, (2002) Heparin-protein interactions. Angew Chem Int Ed Engl 41: 391-412.
62. Hileman RE, Fromm JR, Weiler JM, Linhardt RJ, (1998) Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 20: 156-167.
63. Perriere N, Demeuse P, Garcia E, Regina A, Debray M, et al. (2005) Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93: 279-289.
64. Wang L, Fuster M, Sriramarao P, Esko JD, (2005) Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 6: 902-910.
65. Fuster MM, Wang L, Castagnola J, Sikora L, Reddi K, et al. (2007) Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J Cell Biol 177: 539-549.
66. Sepp KJ, Auld VJ, (2003) Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J Neurosci 23: 8221-8230.