Enhanced adherence to and invasion of PUVEC and PK-15 cells due to the overexpression of RfaD, ThyA and Mip in the ΔompP2 mutant of Haemophilus parasuis SC096 strain

Veterinary Microbiology

Volumn 162, Issue 2-4, 2013, Pages 713-723

  Zhang, Bin ^a,b   Xu, Chenggang ^a   Zhang, Lingyun ^a   Zhou, Suming ^a   Feng, Saixiang ^a   He, Yanbin ^a   Liao, Ming ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b SOUTHWEST UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

ompP2 mutant; Adherence; Comparative proteomic analysis; Haemophilus parasuis; Invasion

Indexed keywords

ADP LEVO GLYCERO DEXTRO MANNOHEPTOSE 6 EPIMERASE; BACTERIAL ENZYME; BACTERIAL PROTEIN; PROTEIN MIP; THYMIDYLATE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CELL ADHESION; CELL INVASION; CELL TYPE; HAEMOPHILUS PARASUIS; HOST CELL; NONHUMAN; PORCINE KIDNEY EPITHELIAL CELL; PORCINE UMBILICUS VEIN ENDOTHELIAL CELL; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CARBOHYDRATE EPIMERASES; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HAEMOPHILUS PARASUIS; PEPTIDYLPROLYL ISOMERASE; SWINE; THYMIDYLATE SYNTHASE;

BACTERIA (MICROORGANISMS); HAEMOPHILUS PARASUIS; NEGIBACTERIA; SUS;

EID: 84872485818     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.09.021     Document Type: Article

References (32)

1. Asanuma N., Yoshizawa K., Kanada K., Hino T. Molecular and biochemical characterization of phosphoenolpyruvate carboxykinase in the ruminal bacterium Ruminococcus albus. Curr. Microbiol. 2009, 58:416-420.
2. Bigas A., Garrido M.E., Badiola I., Barbe J., Llagostera M. Colonization capacity and serum bactericidal activity of Haemophilus parasuis thy mutants. Int. Microbiol. 2006, 9:297-301.
3. Castano-Cerezo S., Pastor J.M., Renilla S., Bernal V., Iborra J.L., Canovas M. An insight into the role of phosphotransacetylase (pta) and the acetate/acetyl-CoA node in Escherichia coli. Microb. Cell. Fact. 2009, 8:54.
4. Chang P.C., Wang C.J., You C.K., Kao M.C. Effects of a HP0859 (rfaD) knockout mutation on lipopolysaccharide structure of Helicobacter pylori 26695 and the bacterial adhesion on AGS cells. Biochem. Biophys. Res. Commun. 2011, 405:497-502.
5. DeMaria T.F., Apicella M.A., Nichols W.A., Leake E.R. Evaluation of the virulence of nontypeable Haemophilus influenzae lipooligosaccharide htrB and rfaD mutants in the chinchilla model of otitis media. Infect. Immun. 1997, 65:4431-4435.
6. Frandoloso R., Martinez-Martinez S., Gutierrez-Martin C.B., Rodriguez-Ferri E.F. Haemophilus parasuis serovar 5 Nagasaki strain adheres and invades PK-15 cells. Vet. Microbiol. 2012, 154:347-352.
7. Herbert M., Kraiss A., Hilpert A.K., Schlor S., Reidl J. Aerobic growth deficient Haemophilus influenzae mutants are non-virulent: implications on metabolism. Int. J. Med. Microbiol. 2003, 293:145-152.
8. Holm M.M., Vanlerberg S.L., Foley I.M., Sledjeski D.D., Lafontaine E.R. The Moraxella catarrhalis porin-like outer membrane protein CD is an adhesin for human lung cells. Infect. Immun. 2004, 72:1906-1913.
9. Iida A., Ohnishi Y., Horinouchi S. Identification and characterization of target genes of the GinI/GinR quorum-sensing system in Gluconacetobacter intermedius. Microbiology 2009, 155:3021-3032.
10. Kielstein P., Rapp-Gabrielson V.J. Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts. J. Clin. Microbiol. 1992, 30:862-865.
11. Klancnik A., Botteldoorn N., Herman L., Mozina S.S. Survival and stress induced expression of groEL and rpoD of Campylobacter jejuni from different growth phases. Int. J. Food Microbiol. 2006, 112:200-207.
12. Leuzzi R., Serino L., Scarselli M., Savino S., Fontana M.R., Monaci E., Taddei A., Fischer G., Rappuoli R., Pizza M. Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol. Microbiol. 2005, 58:669-681.
13. Maeda T., Maeda H., Yamabe K., Mineshiba J., Tanimoto I., Yamamoto T., Naruishi K., Kokeguchi S., Takashiba S. Highly expressed genes in a rough-colony-forming phenotype of Aggregatibacter actinomycetemcomitans: implication of a mip-like gene for the invasion of host tissue. FEMS Immunol. Med. Microbiol. 2010, 58:226-236.
14. Negm R.S., Pistole T.G. The porin OmpC of Salmonella typhimurium mediates adherence to macrophages. Can. J. Microbiol. 1999, 45:658-669.
15. Netzer R., Krause M., Rittmann D., Peters-Wendisch P.G., Eggeling L., Wendisch V.F., Sahm H. Roles of pyruvate kinase and malic enzyme in Corynebacterium glutamicum for growth on carbon sources requiring gluconeogenesis. Arch. Microbiol. 2004, 182:354-363.
16. Oliveira S., Pijoan C. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet. Microbiol. 2004, 99:1-12.
17. Pages J.M., James C.E., Winterhalter M. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat. Rev. Microbiol. 2008, 6:893-903.
18. Ram S., Cullinane M., Blom A.M., Gulati S., McQuillen D.P., Monks B.G., O'Connell C., Boden R., Elkins C., Pangburn M.K., Dahlback B., Rice P.A. Binding of C4b-binding protein to porin: a molecular mechanism of serum resistance of Neisseria gonorrhoeae. J. Exp. Med. 2001, 193:281-295.
19. Reddy M.S., Bernstein J.M., Murphy T.F., Faden H.S. Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect. Immun. 1996, 64:1477-1479.
20. Ross P., O'Gara F., Condon S. Cloning and characterization of the thymidylate synthase gene from Lactococcus lactis subsp. lactis. Appl. Environ. Microbiol. 1990, 56:2156-2163.
21. Sa E.C.C., Griffiths N.J., Virji M. Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS Pathog. 2010, 6:e1000911.
22. Seta F.D., Boschi-Muller S., Vignais M.L., Branlant G. Characterization of Escherichia coli strains with gapA and gapB genes deleted. J. Bacteriol. 1997, 179:5218-5221.
23. Severino V., Chambery A., Vitiello M., Cantisani M., Galdiero S., Galdiero M., Malorni L., Di Maro A., Parente A. Proteomic analysis of human U937 cell line activation mediated by Haemophilus influenzae type b P2 porin and its surface-exposed loop 7. J. Proteome Res. 2010, 9:1050-1062.
24. Vahle J.L., Haynes J.S., Andrews J.J. Interaction of Haemophilus parasuis with nasal and tracheal mucosa following intranasal inoculation of cesarean derived colostrum deprived (CDCD) swine. Can. J. Vet. Res. 1997, 61:200-206.
25. Vanier G., Szczotka A., Friedl P., Lacouture S., Jacques M., Gottschalk M. Haemophilus parasuis invades porcine brain microvascular endothelial cells. Microbiology 2006, 152:135-142.
26. Virji M., Makepeace K., Moxon E.R. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells: the role of integrins in apical interactions. Mol. Microbiol. 1994, 14:173-184.
27. Wagner C., Khan A.S., Kamphausen T., Schmausser B., Unal C., Lorenz U., Fischer G., Hacker J., Steinert M. Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell. Microbiol. 2007, 9:450-462.
28. Xu C., Zhang L., Zhang B., Feng S., Zhou S., Li J., Zou Y., Liao M. Involvement of lipooligosaccharide heptose residues of Haemophilus parasuis SC096 strain in serum resistance, adhesion and invasion. Vet. J. 2012, 10.1016/j.tvjl.2012.06.017.
29. Zhang B., Feng S., Xu C., Zhou S., He Y., Zhang L., Zhang J., Guo L., Liao M. Serum resistance in Haemophilus parasuis SC096 strain requires outer membrane protein P2 expression. FEMS Microbiol. Lett. 2012, 326:109-115.
30. Zhang B., He Y., Xu C., Xu L., Feng S., Liao M., Ren T. Cytolethal distending toxin (CDT) of the Haemophilus parasuis SC096 strain contributes to serum resistance and adherence to and invasion of PK-15 and PUVEC cells. Vet. Microbiol. 2012, 157:237-242.
31. Zhang B., Xu C., Zhou S., Feng S., Zhang L., He Y., Liao M. Comparative proteomic analysis of a Haemophilus parasuis SC096 mutant deficient in the outer membrane protein P5. Microb. Pathog. 2012, 52:117-124.
32. Zhou M., Guo Y., Zhao J., Hu Q., Hu Y., Zhang A., Chen H., Jin M. Identification and characterization of novel immunogenic outer membrane proteins of Haemophilus parasuis serovar 5. Vaccine 2009, 27:5271-5277.