Update on the pathogenesis of Haemophilus parasuis infection and virulence factors

Veterinary Microbiology

Volumn 168, Issue 1, 2014, Pages 1-7

  Zhang, Bin ^a,b   Tang, Cheng ^a   Liao, Ming ^b   Yue, Hua ^a  

^a SOUTHWEST UNIVERSITY FOR NATIONALITIES   (China)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Haemophilus parasuis; Pathogenesis mechanisms; Virulence factors

Indexed keywords

IMMUNOGLOBULIN A; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN P2; PROTEINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERICIDAL ACTIVITY; BACTERIUM ADHERENCE; COMPLEMENT SYSTEM; ENZYME ACTIVITY; HAEMOPHILUS INFECTION; HAEMOPHILUS PARASUIS; HAEMOPHILUS PARASUIS INFECTION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; REVIEW;

HAEMOPHILUS PARASUIS; SUIDAE;

HAEMOPHILUS PARASUIS, PATHOGENESIS MECHANISMS, VIRULENCE FACTORS;

ANIMALS; HAEMOPHILUS INFECTIONS; HAEMOPHILUS PARASUIS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; SWINE; VIRULENCE FACTORS;

EID: 84890798702     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.07.027     Document Type: Review

References (71)

1. Amano H., Shibata M., Takahashi K., Sasaki Y. Effects on endotoxin pathogenicity in pigs with acute septicemia of Haemophilus parasuis infection. J. Vet. Med. Sci. 1997, 59:451-455.
2. Amano A., Takeuchi H., Furuta N. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect. 2010, 12:791-798.
3. Bigas A., Garrido M.E., de Rozas A.M., Badiola I., Barbe J., Llagostera M. Development of a genetic manipulation system for Haemophilus parasuis. Vet. Microbiol. 2005, 105:223-228.
4. Biswas D., Fernando U., Reiman C., Willson P., Potter A., Allan B. Effect of cytolethal distending toxin of Campylobacter jejuni on adhesion and internalization in cultured cells and in colonization of the chicken gut. Avian Dis. 2006, 50:586-593.
5. Bouchet B., Vanier G., Jacques M., Gottschalk M. Interactions of Haemophilus parasuis and its LOS with porcine brain microvascular endothelial cells. Vet. Res. 2008, 39:42.
6. Bouchet B., Vanier G., Jacques M., Auger E., Gottschalk M. Studies on the interactions of Haemophilus parasuis with porcine epithelial tracheal cells: limited role of LOS in apoptosis and pro-inflammatory cytokine release. Microb. Pathog. 2009, 46:108-113.
7. Buckles E.L., Wang X., Lane M.C., Lockatell C.V., Johnson D.E., Rasko D.A., Mobley H.L., Donnenberg M.S. Role of the K2 capsule in Escherichia coli urinary tract infection and serum resistance. J. Infect. Dis. 2009, 199:1689-1697.
8. Cerda-Cuellar M., Aragon V. Serum-resistance in Haemophilus parasuis is associated with systemic disease in swine. Vet. J. 2008, 175:384-389.
9. Chen Y., Jin H., Chen P., Li Z., Meng X., Liu M., Li S., Shi D., Xiao Y., Wang X., Zhou Z., Bi D., Zhou R. Haemophilus parasuis infection activates the NF-κB pathway in PK-15 cells through IκB degradation. Vet. Microbiol. 2012, 160:259-263.
10. Comayras C., Tasca C., Peres S.Y., Ducommun B., Oswald E., De Rycke J. Escherichia coli cytolethal distending toxin blocks the HeLa cell cycle at the G2/M transition by preventing cdc2 protein kinase dephosphorylation and activation. Infect. Immun. 1997, 65:5088-5095.
11. Cope L.D., Pelzel S.E., Latimer J.L., Hansen E.J. Characterization of a mutant of Haemophilus influenzae type b lacking the P2 major outer membrane protein. Infect. Immun. 1990, 58:3312-3318.
12. Costa-Hurtado M., Ballester M., Galofre-Mila N., Darji A., Aragon V. VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages. Vet. Res. 2012, 43:57.
13. DiRienzo J.M., Song M., Wan L.S., Ellen R.P. Kinetics of KB and HEp-2 cell responses to an invasive, cytolethal distending toxin-producing strain of Actinobacillus actinomycetemcomitans. Oral Microbiol. Immunol. 2002, 17:245-251.
14. Fernaays M.M., Lesse A.J., Cai X., Murphy T.F. Characterization of igaB, a second immunoglobulin A1 protease gene in nontypeable Haemophilus influenzae. Infect. Immun. 2006, 74:5860-5870.
15. 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.
16. Galdiero S., Capasso D., Vitiello M., D'Isanto M., Pedone C., Galdiero M. Role of surface-exposed loops of Haemophilus influenzae protein P2 in the mitogen-activated protein kinase cascade. Infect. Immun. 2003, 71:2798-2809.
17. Gibson B.W., Campagnari A.A., Melaugh W., Phillips N.J., Apicella M.A., Grass S., Wang J., Palmer K.L., Munson R.S. Characterization of a transposon Tn916-generated mutant of Haemophilus ducreyi 35000 defective in lipooligosaccharide biosynthesis. J. Bacteriol. 1997, 179:5062-5071.
18. Goodman R.B., Pugin J., Lee J.S., Matthay M.A. Cytokine-mediated inflammation in acute lung injury. Cytokine Growth Factor Rev. 2003, 14:523-535.
19. Gronow S., Brabetz W., Lindner B., Brade H. OpsX from Haemophilus influenzae represents a novel type of heptosyltransferase I in lipopolysaccharide biosynthesis. J. Bacteriol. 2005, 187:6242-6247.
20. Harper M., Cox A.D., St Michael F., Wilkie I.W., Boyce J.D., Adler B. A heptosyltransferase mutant of Pasteurella multocida produces a truncated lipopolysaccharide structure and is attenuated in virulence. Infect. Immun. 2004, 72:3436-3443.
21. Hickey T.E., McVeigh A.L., Scott D.A., Michielutti R.E., Bixby A., Carroll S.A., Bourgeois A.L., Guerry P. Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect. Immun. 2000, 68:6535-6541.
22. Hill C.E., Metcalf D.S., MacInnes J.I. A search for virulence genes of Haemophilus parasuis using differential display RT-PCR. Vet. Microbiol. 2003, 96:189-202.
23. Janowicz D., Luke N.R., Fortney K.R., Katz B.P., Campagnari A.A., Spinola S.M. Expression of OmpP2A and OmpP2B is not required for pustule formation by Haemophilus ducreyi in human volunteers. Microbial. Pathog. 2006, 40:110-115.
24. Jennings M.P., Bisercic M., Dunn K.L., Virji M., Martin A., Wilks K.E., Richards J.C., Moxon E.R. Cloning and molecular analysis of the Isi1 (rfaF) gene of Neisseria meningitidis which encodes a heptosyl-2-transferase involved in LPS biosynthesis: evaluation of surface exposed carbohydrates in LPS mediated toxicity for human endothelial cells. Microb. Pathog. 1995, 19:391-407.
25. Kanipes M.I., Holder L.C., Corcoran A.T., Moran A.P., Guerry P. A deep-rough mutant of Campylobacter jejuni 81-176 is noninvasive for intestinal epithelial cells. Infect. Immun. 2004, 72:2452-2455.
26. 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.
27. Klena J.D., Gray S.A., Konkel M.E. Cloning, sequencing, and characterization of the lipopolysaccharide biosynthetic enzyme heptosyltransferase I gene (waaC) from Campylobacter jejuni and Campylobacter coli. Gene 1998, 222:177-185.
28. Lara-Tejero M., Galan J.E. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect. Immun. 2001, 69:4358-4365.
29. Li H., Wang L.Y., Xu G.Y., Chen Y., Jiang R., Li Y. Cloning, expression and characterization of the Ste6 gene encoding a UDP-glucose dehydrogenase in Streptomyces. Yi Chuan Xue Bao 2005, 32:1213-1220.
30. Melnikow E., Dornan S., Sargent C., Duszenko M., Evans G., Gunkel N., Selzer P.M., Ullrich H.J. Microarray analysis of Haemophilus parasuis gene expression under in vitro growth conditions mimicking the in vivo environment. Vet. Microbiol. 2005, 110:255-263.
31. Mullins M.A., Register K.B., Bayles D.O., Loving C.L., Nicholson T.L., Brockmeier S.L., Dyer D.W., Phillips G.J. Characterization and comparative analysis of the genes encoding Haemophilus parasuis outer membrane proteins P2 and P5. J. Bacteriol. 2009, 191:5988-6002.
32. Mullins M.A., Register K.B., Bayles D.O., Butler J.E. Haemophilus parasuis exhibits IgA protease activity but lacks homologs of the IgA protease genes of Haemophilus influenzae. Vet. Microbiol. 2011, 153:407-412.
33. Mullins M.A., Register K.B., Bayles D.O., Dyer D.W., Kuehn J.S., Phillips G.J. Genome sequence of Haemophilus parasuis strain 29755. Stand. Genomic Sci. 2011, 5:61-68.
34. Naito M., Frirdich E., Fields J.A., Pryjma M., Li J., Cameron A., Gilbert M., Thompson S.A., Gaynor E.C. Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J. Bacteriol. 2010, 192:2182-2192.
35. Oliveira S., Pijoan C. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet. Microbiol. 2004, 99:1-12.
36. Olvera A., Ballester M., Nofrarias M., Sibila M., Aragon V. Differences in phagocytosis susceptibility in Haemophilus parasuis strains. Vet. Res. 2009, 40:24.
37. Pina S., Olvera A., Barcelo A., Bensaid A. Trimeric autotransporters of Haemophilus parasuis: generation of an extensive passenger domain repertoire specific for pathogenic strains. J. Bacteriol. 2009, 191:576-587.
38. Ram S., McQuillen D.P., Gulati S., Elkins C., Pangburn M.K., Rice P.A. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 1998, 188:671-680.
39. Ramjeet M., Cox A.D., Hancock M.A., Mourez M., Labrie J., Gottschalk M., Jacques M. Mutation in the LPS outer core biosynthesis gene, galU, affects LPS interaction with the RTX toxins ApxI and ApxII and cytolytic activity of Actinobacillus pleuropneumoniae serotype 1. Mol. Microbiol. 2008, 70:221-235.
40. Rautemaa R., Meri S. Complement-resistance mechanisms of bacteria. Microbes Infect. 1999, 1:785-794.
41. 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.
42. Ruiz A., Oliveira S., Torremorell M., Pijoan C. Outer membrane proteins and DNA profiles in strains of Haemophilus parasuis recovered from systemic and respiratory sites. J. Clin. Microbiol. 2001, 39:1757-1762.
43. 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 Pathogens 2010, 6:e1000911.
44. Serruto D., Rappuoli R., Scarselli M., Gros P., van Strijp J.A. Molecular mechanisms of complement evasion: learning from staphylococci and meningococci. Nat. Rev. Microbiol. 2010, 8:393-399.
45. Shenker B.J., Besack D., McKay T., Pankoski L., Zekavat A., Demuth D.R. Actinobacillus actinomycetemcomitans cytolethal distending toxin (Cdt): evidence that the holotoxin is composed of three subunits: CdtA, CdtB, and CdtC. J. Immunol. 2004, 172:410-417.
46. Stevens M.K., Latimer J.L., Lumbley S.R., Ward C.K., Cope L.D., Lagergard T., Hansen E.J. Characterization of a Haemophilus ducreyi mutant deficient in expression of cytolethal distending toxin. Infect. Immun. 1999, 67:3900-3908.
47. Swords W.E., Buscher B.A., Ver Steeg Ii K., Preston A., Nichols W.A., Weiser J.N., Gibson B.W., Apicella M.A. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 2000, 37:13-27.
48. Tadjine M., Mittal K.R., Bourdon S., Gottschalk M. Development of a new serological test for serotyping Haemophilus parasuis isolates and determination of their prevalence in North America. J. Clin. Microbiol. 2004, 42:839-840.
49. Tadjine M., Mittal K.R., Bourdon S., Gottschalk M. Production and characterization of murine monoclonal antibodies against Haemophilus parasuis and study of their protective role in mice. Microbiology 2004, 150:3935-3945.
50. 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.
51. 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.
52. Vilches S., Canals R., Wilhelms M., Salo M.T., Knirel Y.A., Vinogradov E., Merino S., Tomas J.M. Mesophilic Aeromonas UDP-glucose pyrophosphorylase (GalU) mutants show two types of lipopolysaccharide structures and reduced virulence. Microbiology 2007, 153:2393-2404.
53. Vitiello M., Finamore E., Cantisani M., Bevilacqua P., Incoronato N., Falanga A., Galdiero E., Galdiero M. P2 porin and loop L7 from Haemophilus influenzae modulate expression of IL-6 and adhesion molecules in astrocytes. Microbiol. Immunol. 2011, 55:347-356.
54. Vitovski S., Read R.C., Sayers J.R. Invasive isolates of Neisseria meningitidis possess enhanced immunoglobulin A1 protease activity compared to colonizing strains. FASEB J. 1999, 13:331-337.
55. Vuong C., Kocianova S., Voyich J.M., Yao Y., Fischer E.R., DeLeo F.R., Otto M. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 2004, 279:54881-54886.
56. Wang X., Xu X., Zhang S., Guo F., Cai X., Chen H. Identification and analysis of potential virulence-associated genes in Haemophilus parasuis based on genomic subtraction. Microb. Pathog. 2011, 51:291-296.
57. Wang Y., Liu C., Fang Y., Liu X., Li W., Liu S., Liu Y., Charreyre C., Audonnet J.C., Chen P., He Q. Transcription analysis on response of porcine alveolar macrophages to Haemophilus parasuis. BMC Genomics 2012, 13:68.
58. Wang X., Xu X., Wu Y., Li L., Cao R., Cai X., Chen H. Polysaccharide biosynthesis protein CapD is a novel pathogenicity-associated determinant of Haemophilus parasuis involved in serum-resistance ability. Vet. Microbiol. 2013, 164:184-189.
59. Woof J.M., Kerr M.A. The function of immunoglobulin A in immunity. J. Pathol. 2006, 208:270-282.
60. Xie Q., Jin H., Luo R., Wan Y., Chu J., Zhou H., Shi B., Chen H., Zhou R. Transcriptional responses of Haemophilus parasuis to iron-restriction stress in vitro. Biometals 2009, 22:907-916.
61. Xu Z., Yue M., Zhou R., Jin Q., Fan Y., Bei W., Chen H. Genomic characterization of Haemophilus parasuis SH0165, a highly virulent strain of serovar 5 prevalent in China. PLoS One 2011, 6:e19631.
62. 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. 2013, 195:200-204.
63. Yue M., Yang F., Yang J., Bei W., Cai X., Chen L., Dong J., Zhou R., Jin M., Jin Q., Chen H. Complete genome sequence of Haemophilus parasuis SH0165. J. Bacteriol. 2009, 191:1359-1360.
64. 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.
65. 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.
66. Zhang B., Xu C., Liao M. Outer membrane protein P2 of the Haemophilus parasuis SC096 strain contributes to adherence to porcine alveolar macrophages cells. Vet. Microbiol. 2012, 158:226-227.
67. Zhao Q., Tang C., Yang F., Shao G., Yue H. The correlation between structural characterization of ompP2 gene and virulence of Haemophilus parasuis. Sci. Sin. 2010, 6:522-532. (in Chinese).
68. 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.
69. Zhou H., Yang B., Xu F., Chen X., Wang J., Blackall P.J., Zhang P., Xia Y., Zhang J., Ma R. Identification of putative virulence-associated genes of Haemophilus parasuis through suppression subtractive hybridization. Vet. Microbiol. 2010, 144:377-383.
70. Zhou M., Zhang Q., Zhao J., Jin M. Haemophilus parasuis encodes two functional cytolethal distending toxins: CdtC contains an atypical cholesterol recognition/interaction region. PLoS One 2012, 7:e32580.
71. Zou Y., Feng S., Xu C., Zhang B., Zhou S., Zhang L., He X., Li J., Yang Z., Miao M. The role of galU and galE of Haemophilus parasuis SC096 in serum resistance and biofilmformation. Vet. Microbiol. 2013, 162:278-284.