O-polysaccharide glycosylation is required for stability and function of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans

Infection and Immunity

Volumn 80, Issue 8, 2012, Pages 2868-2877

  Tang, Gaoyan ^a   Ruiz, Teresa ^b   Mintz, Keith P ^a  

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

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACITRACIN; COLLAGEN; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; O POLYSACCHARIDE; POLYSACCHARIDE; PROTEIN APIA; PROTEIN EMAA; PYROPHOSPHATE; UNCLASSIFIED DRUG;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL STRAIN; BIOGENESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION;

ADHESINS, BACTERIAL; ANTI-BACTERIAL AGENTS; BACITRACIN; CELL MEMBRANE; COLLAGEN; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOSYLATION; LIPOPOLYSACCHARIDES; MICROSCOPY, ELECTRON, TRANSMISSION; O ANTIGENS; PASTEURELLACEAE; PROTEIN BINDING;

EID: 84864809139     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00372-12     Document Type: Article

References (37)

1. Azari F, Radermacher M, Mintz K, Ruiz T. 2012. Correlation of the amino-acid sequence and the 3D structure of the functional domain of EmaA from Aggregatibacter actinomycetemcomitans. J. Struct. Biol. 177: 439-446.
2. Benz I, Schmidt M. 2002. Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol. 45:267-276.
3. Braakman I, Bulleid N. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80:71-99.
4. Charbonneau M, et al. 2007. O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J. Bacteriol. 189:8880-8889.
5. Gallant C, Sedic M, Chicoine E, Ruiz T, Mintz K. 2008. Membrane morphology and leukotoxin secretion are associated with a novel membrane protein of Aggregatibacter actinomycetemcomitans. J. Bacteriol. 190: 5972-5980.
6. Gur E, Biran D, Ron E. 2011. Regulated proteolysis in Gram-negative bacteria: how and when? Nat. Rev. Microbiol. 9:839-848.
7. Hagan C, Silhavy T, Kahne D. 2011. _-Barrel membrane protein assembly by the Bam complex. Annu. Rev. Biochem. 80:189 -210.
8. Henderson I, Navarro-Garcia F, Desvaux M, Fernandez R, Ala'Aldeen D. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
9. Hug I, Feldman M. 2011. Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria. Glycobiology 21:138 -151.
10. Inoue T, Ohta H, Tanimoto I, Shingaki R, Fukui K. 2000. Heterogeneous post-translational modification of Actinobacillus actinomycetemcomitans fimbrillin. Microbiol. Immunol. 44:715-718.
11. Jiang X, Ruiz T, Mintz K. 2011. The extended signal peptide of the trimeric autotransporter EmaA of Aggregatibacter actinomycetemcomitans modulates secretion. J. Bacteriol. 193:6983- 6994.
12. Kachlany S, Planet P, DeSalle R, Fine D, Figurski D. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol. 9:429-437.
13. Komatsuzawa H, et al. 2002. Identification of six major outer membrane proteins from Actinobacillus actinomycetemcomitans. Gene 288:195-201.
14. Larkin A, Imperiali B. 2011. The expanding horizons of asparaginelinked glycosylation. Biochemistry 50:4411- 4426.
15. Merkx-Jacques A, Obhi R, Bethune G, Creuzenet C. 2004. The Helicobacter pylori flaA1 and wbpB genes control lipopolysaccharide and flagellum synthesis and function. J. Bacteriol. 186:2253-2265.
16. Mintz K. 2004. Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 150:2677-2688.
17. Ouhara K, et al. 2006. Actinobacillus actinomycetemcomitans outer membrane protein 100 triggers innate immunity and production of betadefensin and the 18-kilodalton cationic antimicrobial protein through the fibronectin-integrin pathway in human gingival epithelial cells. Infect. Immun. 74:5211-5220.
18. Paramonov N, et al. 2005. Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arggingipain glycans. Mol. Microbiol. 58:847- 863.
19. Pérez J, McGarry M, Marolda C, Valvano M. 2008. Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol. Microbiol. 70:1424 -1440.
20. Potron A, et al. 2010. Recurrent infective endocarditis due to Aggregatibacter actinomycetemcomitans: reinfection or relapse? J. Med. Microbiol. 59:1524 -1526.
21. Power P, et al. 2003. Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis. Mol. Microbiol. 49:833- 847.
22. Raetz C, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
23. Rahamat-Langendoen J, et al. 2011. Brain abscess associated with Aggregatibacter actinomycetemcomitans: case report and review of literature. J. Clin. Periodontol. 38:702-706.
24. Rose J, Meyer D, Fives-Taylor P. 2003. Aae, an autotransporter involved in adhesion of Actinobacillus actinomycetemcomitans to epithelial cells. Infect. Immun. 71:5284 -5293.
25. Ruiz T, Lenox C, Radermacher M, Mintz K. 2006. Novel surface structures are associated with the adhesion of Actinobacillus actinomycetemcomitans to collagen. Infect. Immun. 74:6163- 6170.
26. Schmidt M, Riley L, Benz I. 2003. Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol. 11:554 -561.
27. Scott A, et al. 2011. Flagellar glycosylation in Burkholderia pseudomallei and Burkholderia thailandensis. J. Bacteriol. 193:3577-3587.
28. Szymanski C, Burr D, Guerry P. 2002. Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70:2242-2244.
29. Tabei S, et al. 2009. An Aeromonas caviae genomic island is required for both O-antigen lipopolysaccharide biosynthesis and flagellin glycosylation. J. Bacteriol. 191:2851-2863.
30. Tang G, Kawai T, Komatsuzawa H, Mintz K. 2012. Lipopolysaccharides mediate leukotoxin secretion in Aggregatibacter actinomycetemcomitans. Mol. Oral Microbiol. 27:70-82.
31. Tang G, Kitten T, Munro C, Wellman G, Mintz K. 2008. EmaA, a potential virulence determinant of Aggregatibacter (Actinobacillus) actinomycetemcomitans in infective endocarditis. Infect. Immun. 76:2316 -2324.
32. Tang G, Mintz K. 2010. Glycosylation of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans is dependent upon the lipopolysaccharide biosynthetic pathway J. Bacteriol. 192:1395-1404.
33. Tang G, Ruiz T, Barrantes-Reynolds R, Mintz K. 2007. Molecular heterogeneity of EmaA, an oligomeric autotransporter adhesin of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Microbiology 153: 2447-2457.
34. Tomich M, Fine D, Figurski D. 2006. The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J. Bacteriol. 188:6899-6914.
35. Yoshida Y, Nakano Y, Nezu T, Yamashita Y, Koga T. 1999. A novel NDP-6-deoxyhexosyl-4-ulose reductase in the pathway for the synthesis of thymidine diphosphate-D-fucose. J. Biol. Chem. 274:16933-16939.
36. Yu C, Ruiz T, Lenox C, Mintz K. 2008. Functional mapping of an oligomeric autotransporter adhesin of Aggregatibacter actinomycetemcomitans. J. Bacteriol. 190:3098 -3109.
37. Yue G, Kaplan J, Furgang D, Mansfield K, Fine D. 2007. A second Aggregatibacter actinomycetemcomitans autotransporter adhesin exhibits specificity for buccal epithelial cells in humans and old world primates. Infect. Immun. 75:4440-4448.