Signature-tagged mutagenesis of Pasteurella multocida identifies mutants displaying differential virulence characteristics in mice and chickens

Infection and Immunity

Volumn 71, Issue 9, 2003, Pages 5440-5446

  Harper, Marina ^a   Boyce, John D ^a   Wilkie, Ian W ^b   Adler, Ben ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

ARTICLE; ATTENUATION; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CHICKEN; CHOLERA; CONTROLLED STUDY; FEMALE; GENE INSERTION; MOUSE; MUTAGENESIS; NONHUMAN; PASTEURELLA MULTOCIDA; PRIORITY JOURNAL; SEPTICEMIA;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL MEMBRANE; CHICKENS; CLONING, MOLECULAR; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; FEMALE; GENES, BACTERIAL; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MUTAGENESIS, INSERTIONAL; PASTEURELLA INFECTIONS; PASTEURELLA MULTOCIDA; SEPSIS; SEQUENCE TAGGED SITES; SPECIES SPECIFICITY; VIRULENCE;

EID: 0041823270     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.9.5440-5446.2003     Document Type: Article

References (48)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1995. Current protocols in molecular biology, vol. 1. John Wiley & Sons, Inc., New York, N.Y.
3. Badger, J. L., C. A. Wass, S. J. Weissman, and K. S. Kim. 2000. Application of signature-tagged mutagenesis for identification of Escherichia coli K1 genes that contribute to invasion of human brain microvascular endothelial cells. Infect. Immun. 68:5056-5061.
4. Berryman, D. I., and J. I. Rood. 1995. The closely related ermB-ermAM genes from Clostridium perfringens, Enterococcus faecalis (pAMβ1), and Streptococcus agalactiae (pIP501) are flanked by variants of a directly repeated sequence. Antimicrob. Agents Chemother. 39:1830-1834.
5. Black, P. N., B. Said, C. R. Ghosn, J. V. Beach, and W. D. Nunn. 1987. Purification and characterization of an outer membrane-bound protein involved in long-chain fatty acid transport in Escherichia coli. J. Biol. Chem. 262:1412-1419.
6. Bosch, M., E. Garrido, M. Llagostera, A. M. P. de Rozas, I. Badiola, and J. Barbe. 2002. Pasteurella multocida exbB, exbD and tonB genes are physically linked but independently transcribed. FEMS Microbiol. Lett. 210:201-208.
7. Boyce, J. D., and B. Adler. 2000. The capsule is a virulence determinant in the pathogenesis of Pasteurella multocida M1404 (B:2). Infect. Immun. 68:3463-3468.
8. Boyce, J. D., I. Wilkie, M. Harper, M. L. Paustian, V. Kapur, and B. Adler. 2002. Genomic scale analysis of Pasteurella multocida gene expression during growth within the natural chicken host. Infect. Immun. 70:6871-6879.
9. Chiang, S. L., and J. J. Mekalanos. 1998. Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol. Microbiol. 27:797-805.
10. Chung, J. Y., I. Wilkie, J. D. Boyce, K. M. Townsend, A. J. Frost, M. Ghoddusi, and B. Adler. 2001. Role of capsule in the pathogenesis of fowl cholera caused by Pasteurella multocida serogroup A. Infect. Immun. 69:2487-2492.
11. Coulter, S. N., W. R. Schwan, E. Y. Ng, M. H. Langhorne, H. D. Ritchie, S. Westbrock-Wadman, W. O. Hufnagle, K. R. Folger, A. S. Bayer, and C. K. Stover. 1998. Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol. Microbiol. 30:393-404.
12. Cox, A. D., J. C. Wright, J. Li, D. W. Hood, E. R. Moxon, and J. C. Richards. 2003. Phosphorylation of the lipid a region of meningococcal lipopolysaccharide: identification of a family of transferases that add phosphoethanolamine to lipopolysaccharide. J. Bacteriol. 185:3270-3277.
13. Darwin, A. J., and V. L. Miller. 1999. Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature-tagged transposon mutagenesis. Mol. Microbiol. 32:51-62.
14. DeAngelis, P. L. 1998. Transposon Tn916 insertional mutagenesis of Pasteurella multocida and direct sequencing of disruption site. Microb. Pathog. 24:203-209.
15. Filiatrault, M. J., B. W. Gibson, B. Schilling, S. H. Sun, R. S. Munson, and A. A. Campagnari. 2000. Construction and characterization of Haemophilus ducreyi lipooligosaccharide (LOS) mutants defective in expression of heptosyltransferase III and β1, 4-glucosyltransferase: identification of LOS glycoforms containing lactosamine repeats. Infect. Immun. 68:3352-3361.
16. Foged, N. T., J. P. Nielsen, and S. E. Jorsal. 1989. Protection against progressive atrophic rhinitis by vaccination with Pasteurella multocida toxin purified by monoclonal antibodies. Vet. Rec. 125:7-11.
17. Fuller, T. E., M. J. Kennedy, and D. E. Lowery. 2000. Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb. Pathog. 29:25-38.
18. Gawron-Burke, C., and D. B. Clewell. 1984. Regeneration of insertionally inactivated streptococcal DNA fragments after excision of transposon Tn916 in Escherichia coli: strategy for targeting and cloning of genes from gram-positive bacteria. J. Bacteriol. 159:214-221.
19. Hansen, E. J., S. M. Robertson, P. A. Gulig, C. F. Frisch, and E. J. Haanes. 1982. Immunoprotection of rats against Haemophilus influenzae type B disease mediated by monoclonal antibody against a haemophilus outer-membrane protein. Lancet i:366-368.
20. Hensel, M., J. E. Shea, C. Gleeson, M. D. Jones, E. Dalton, and D. W. Holden. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400-403.
21. Hood, D. W., M. E. Deadman, M. P. Jennings, M. Bisercic, R. D. Fleischmann, J. C. Venter, and E. R. Moxon. 1996. DNA repeats identify novel virulence genes in Haemophilus influenzae. Proc. Natl. Acad. Sci. USA 93:11121-11125.
22. Hunt, M. L., D. J. Boucher, J. D. Boyce, and B. Adler. 2001. In vivo-expressed genes of Pasteurella multocida. Infect. Immun. 69:3004-3012.
23. Isaacson, R. E., and E. Trigo. 1995. Pili of Pasteurella multocida of porcine origin. FEMS Microbiol. Lett. 132:247-251.
24. Kachlany, S. C., P. J. Planet, M. K. Bhattacharjee, E. Kollia, R. DeSalle, D. H. Fine, and D. H. Figurski. 2000. Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in bacteria and archaea. J. Bacteriol. 182:6169-6176.
25. Kachlany, S. C., P. J. Planet, R. DeSalle, D. H. Fine, D. H. Figurski, and J. B. Kaplan. 2001. flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol. Microbiol. 40:542-554.
26. Lau, G. W., S. Haataja, M. Lonetto, S. E. Kensit, A. Marra, A. P. Bryant, D. McDevitt, D. A. Morrison, and D. W. Holden. 2001. A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol. Microbiol. 40:555-571.
27. Loeb, M. R. 1987. Protection of infant rats from Haemophilus influenzae type b infection by antiserum to purified outer membrane protein a. Infect Immun. 55:2612-2618.
28. Mackinnon, F. G., A. D. Cox, J. S. Plested, C. M. Tang, K. Makepeace, P. A. Coull, J. C. Wright, R. Chalmers, D. W. Hood, J. C. Richards, and E. R. Moxon. 2002. Identification of a gene (lpt-3) required for the addition of phosphoethanolamine to the lipopolysaccharide inner core of Neisseria meningitidis and its role in mediating susceptibility to bactericidal killing and opsonophagocytosis. Mol. Microbiol. 43:931-943.
29. Maloy, S. R., C. L. Ginsburgh, R. W. Simons, and W. D. Nunn. 1981. Transport of long and medium chain fatty acids by Escherichia coli K12. J. Biol. Chem. 256:3735-3742.
30. Mannheim, W. 1984. Family III. Pasteurellaceae, p. 550-575. In N. R. Krieg and J. G. Kolt (ed.), Bergey's manual of systematic bacteriology, vol. 1. Williams & Wilkins, Baltimore, Md.
31. May, B. J., Q. Zhang, L. L. Li, M. L. Paustian, T. S. Whittam, and V. Kapur. 2001. Complete genomic sequence of Pasteurella multocida, Pm70. Proc. Natl. Acad. Sci. USA 98:3460-3465.
32. Mortensen, L., G. Dandanell, and K. Hammer. 1989. Purification and characterization of the DeoR repressor of Escherichia coli. EMBO J. 8:325-331.
33. Munson, R., Jr., and A. Hunt. 1989. Isolation and characterization of a mutant of Haemophilus influenzae type b deficient in outer membrane protein P1. Infect. Immun. 57:1002-1004.
34. Neuhard, J., and R. A. Kellin. 1996. Biosynthesis and conversions of pyrimidines, p. 580-599. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington D.C.
35. Nunn, W. D., and R. W. Simons. 1978. Transport of long-chain fatty acids by Escherichia coli: mapping and characterization of mutants in the fadL gene. Proc. Natl. Acad. Sci. USA 75:3377-3381.
36. Ochman, H., A. S. Gerber, and D. L. Hartl. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623.
37. Park, J. T. 1996. The murein sacculus, p. 48-57. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology., 2nd ed., vol. 1. ASM Press, Washington, D.C.
38. Phillips, N. J., M. A. Apicella, J. M. Griffiss, and B. W. Gibson. 1992. Structural characterization of the cell surface lipooligosaccharides from a nontypable strain of Haemophilus influenzae. Biochemistry 31:4515-4526.
39. Phillips, N. J., M. A. Apicella, J. M. Griffiss, and B. W. Gibson. 1993. Structural studies of the lipooligosaccharides from Haemophilus influenzae type b strain A2. Biochemistry 32:2003-2012.
40. Pruimboom, I. M., R. B. Rimler, and M. R. Ackermann. 1999. Enhanced adhesion of Pasteurella multocida to cultured turkey peripheral blood monocytes. Infect. Immun. 67:1292-1296.
41. Pruimboom, I. M., R. B. Rimler, M. R. Ackermann, and K. A. Brogden. 1996. Capsular hyaluronic acid-mediated adhesion of Pasteurella multocida to turkey air sac macrophages. Avian Dis. 40:887-893.
42. Rebers, P. A., A. E. Jensen, and G. A. Laird. 1988. Expression of pili and capsule by the avian strain P-1059 of Pasteurella multocida. Avian Dis. 32:313-318.
43. Rhoades, K. R., and R. B. Rimler. 1990. Pasteurella multocida colonization and invasion in experimentally exposed turkey poults. Avian Dis. 34:381-383.
44. Ruffolo, C. G., J. M. Tennent, W. P. Michalski, and B. Adler. 1997. Identification, purification, and characterization of the type 4 fimbriae of Pasteurella multocida. Infect. Immun. 65:339-343.
45. Schiffer, G., and J. V. Holtje. 1999. Cloning and characterization of PBP1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274:32031-32039.
46. Segada, L. M., G. M. Carlone, L. L. Gheesling, and A. J. Lesse. 2000. Characterization of P1-deficient isogenic mutant of Haemophilus influenzae biogroup aegyptius associated with Brazilian purpuric fever. Microb. Pathog. 28:145-155.
47. Tsolis, R. M., S. M. Townsend, E. A. Miao, S. I. Miller, T. A. Ficht, L. G. Adams, and A. J. Baumler. 1999. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect. Immun. 67:6385-6393.
48. Zalkin, H., and P. Nygaard. 1996. Biosynthesis of purine nucleotides, p. 561-579. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.