Type 4 Pili in the Families Moraxellaceae and Neisseraceae

Carl F. Marrs

doi:10.1128/9781555818340.ch9

Chapter 9 : Type 4 Pili in the Families Moraxellaceae and Neisseraceae

Author: Carl F. Marrs¹

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, Michigan 48109

Content Type: Monograph

Publication Year: 1994

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

Book DOI: 10.1128/9781555818340

Chapter DOI: 10.1128/9781555818340.ch9

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Type 4 Pili in the Families Moraxellaceae and Neisseraceae, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap09-2.gif

Abstract:

This chapter reviews studies on type 4 pili from the species Moraxella bovis, Moraxella lacunata, and Moraxella nonliquefaciens of the family Moraxellaceae and Eikenella corrodens, Kingella denitrificans, and Kingella kingae of the family Neisseriaceae. K. kingae was originally classified as Moraxella kingii and was then transferred to the new genus Kingella within the family Neisseriaceae in 1976. Further studies with M. nonliquefaciens, M. bovis, and M. kingii confirmed the association between the "spreading-corroding" (SC) colony type and piliation. Researchers studied thin sections of M. bovisin the electron microscope and concluded that the pili were distributed peritrichously around the cell. When M. bovis Epp63 was propagated on 5% sheep blood agar, one N-type and six distinct piliated colony types were observed. Thus, pellicle formation can be used as an enrichment procedure to isolate the often rare variants switching from the nonpiliated to the piliated state. The competence for DNA transformation in piliated E. corrodens has also been demonstrated. Further studies on the function and genetics of type 4 pili may lead to a better understanding of the roles that they play in so many bacterial species.

Citation: Marrs C. 1994. Type 4 Pili in the Families Moraxellaceae and Neisseraceae, p 127-143. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch9

Key Concept Ranking

Bacterial Pathogenesis: 0.70707446
Type IV Pili: 0.42164052

0.70707446

Highlighted Text: Show | Hide

Full text loading...

Figures

Type 4 Pili in the Families Moraxellaceae and Neisseraceae

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818340.chap9-1,webId=/content/author/10.1128/9781555818340.chap9-1,properties={foaf_givenname=Carl F., foaf_name=Carl F. Marrs, foaf_surname=Marrs, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818340.chap9-aff1]]}]]

/content/10.1128/9781555818340.chap9.fig9-1

Figure 1

SC and N colony types of M. bovis on bovine blood agar (A) or GC agar medium (B). (A) The SC colonies exhibit a “fried egg” appearance, while the N colony is relatively featureless. (B) The SC colonies are small and domed, while the N colony is much larger.

10.1128/9781555818340/fig9-1_thmb.gif

10.1128/9781555818340/fig9-1.gif

Figure 1

/content/10.1128/9781555818340.chap9.fig9-2

Figure 2

(A) Diagram of the M. bovis pilin gene inversion region in orientation 1, with tfpQ in the expression locus. Parentheses represent the sites of inversion, and lines beneath the map show the direction of transcription (dashed lines indicate genes for which we have no evidence of transcription). (B) The same region in orientation 2, with tfpI in the expression locus.

10.1128/9781555818340/fig9-2_thmb.gif

10.1128/9781555818340/fig9-2.gif

Figure 2

/content/10.1128/9781555818340.chap9.fig9-3

Figure 3

Comparison of the pilin gene inversion regions of M. bovis and M. lacunata. The hatched region of tfpB represents the portion of the gene present in M. bovis but absent from M. lacunata.

10.1128/9781555818340/fig9-3_thmb.gif

10.1128/9781555818340/fig9-3.gif

Figure 3

Comparison of the pilin gene inversion regions of M. bovis and M. lacunata. The hatched region of tfpB represents the portion of the gene present in M. bovis but absent from M. lacunata.

/content/10.1128/9781555818340.chap9.fig9-4

Figure 4

(A) Diagram of the arrangement of two pilin genes and a hemagglutinin gene from the E. corrodens type strain ATCC 23834. (B) Similar genes from E. corrodens 31745. The region past ecpD does not contain a gene equivalent to the hemagglutinin gene found in the type strain. The arrows below the genes show the directions of transcription.

10.1128/9781555818340/fig9-4_thmb.gif

10.1128/9781555818340/fig9-4.gif

Figure 4

References

/content/book/10.1128/9781555818340.chap9

1. Adachi, R.,, O. Hammerberg,, and H. Richardson. 1983. Infective endocarditis caused by Kingella kingae. Can. Med. Assoc. J. 128: 1087– 1088.

2. Amir, J.,, and P. G. Shockelford. 1991. Kingella kingae intervertebral disk infection. J. Clin. Microbiol. 29: 1083– 1086.

3. Baptista, P. J. H. P. 1979. Infectious bovine keratoconjunctivitis: a review. Br. Vet. J. 135: 225– 242.

4. Barner, R. D. 1952. A study of Moraxella bovis and its relation to bovine keratitis. Am. J. Vet. Res. 13: 132– 144.

5. Baum, J.,, H. B. Fedukowicz,, and A. Jordan. 1980. A survey of Moraxella corneal ulcers in a derelict population. Am. J. Ophthalmol. 90: 476– 480.

6. Beard, M. K. M.,, J. S. Mattick,, L. J. Moore,, M. R. Mott,, C. F. Marrs,, and J. R. Egerton. 1990. Morphogenetic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa. J. Bacteriol. 172: 2601– 2607.

7. Bosworth, D. E. 1983. Kingella (Moraxella) kingae infections in children. Am. J. Dis. Child. 137: 650– 653.

8. Bottone, E.,, and J. Allerhand. 1968. Association of mucoid encapsulated Moraxella duplex var. nonliquefaciens with chronic bronchitis. Appl. Microbiol. 16: 315– 319.

9. Bovre, K. 1965. Studies on transformation in Moraxella and organisms assumed to be related to Moraxella. 3. Quantitative streptomycin resistance transformation between Moraxella bovis and Moraxella nonliquefaciens strains. Acta Pathol. Microbiol. Scand. 63: 42– 50.

10. Bovre, K. 1970. Pulse-RNA-DNA hybridization between rodshaped and coccal species of the Moraxella-Neisseria groups. Acta Pathol. Microbiol. Scand. Sect. B 78: 565– 574.

11. Bovre, K. 1970. Oxidase positive bacteria in the human nose. Incidence and species distribution as diagnosed by genetic transformation. Acta Pathol. Microbiol. Scand. Sect. B 78: 780– 784.

12. Bovre, K.,, T. Bergan,, and L. O. Froholm. 1970. Electron microscopical and serological characteristics associated with colony type in Moraxella nonliquefaciens. Acta Pathol. Microbiol. Scand. Sect. B 78: 765– 779.

13. Bovre, K.,, and L. O. Froholm. 1970. Correlation between the fimbriated state and competence of genetic transformation in Moraxella nonliquefaciens strains. Acta Pathol. Microbiol. Scand. Sect. B 78: 526– 528.

14. Bovre, K.,, and L. O. Froholm. 1971. Competence of genetic transformation correlated with the occurrence of fimbriae in three bacterial species. Nature (London) New Biol. 234: 151– 152.

15. Bovre, K.,, and L. O. Froholm. 1972. Variation of colony morphology reflecting fimbriation in Moraxella bovis and two reference strains of Moraxella nonliquefaciens. Acta Pathol. Microbiol. Scand. Sect. B 80: 629– 640.

16. Bovre, K.,, and L. O. Froholm. 1972. Competence in genetic transformation related to colony type and fimbriation in three species of Moraxella. Acta Pathol. Microbiol. Scand. Sect. B 80: 649– 659.

17. Bovre, K.,, and N. Hagen,. 1981. The family Neisseriaceae: rod-shaped species of the genera Moraxella, Acinetobacter, Kingella, and Neisseria, and the Branhamella group of cocci, p. 1506– 1529. In M. P. Starr,, H. Stolp,, H. G. Truper,, A. Balows,, and H. G. Schlegel (ed.), The Prokaryotes: a Handbook on Habitats, Isolation, and Identification of Bacteria. Springer-Verlag, New York..

18. Bradley, D. E. 1974. The adsorption of Pseudomonas aeruginosa pilus-dependent bacteriophages to a host mutant with nonretractile pili. Virology 58: 149– 163.

19. Bradley, D. E. 1980. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can. J. Microbiol. 26: 146– 154.

20. Brill, C. B.,, L. S. Pearlstein,, J. M. Kaplan,, and E. L. Mancall. 1982. CNS infections caused by Eikenella corrodens. Arch. Neurol. 39: 431– 432.

21. Brown, A. M.,, M. M. Rothburn,, C. Roberts,, and F. J. Nye. 1987. Septicaemia with probable endocarditis caused by Kingella denitrificans. J. Infect. 15: 225– 228.

22. Chanal, C.,, F. Tiget,, P. Chapuis,, D. Campagne,, M. Jan, and J. Sirot. 1987. Spondylitis and osteomyelitis caused by Kingella kingae in children. J. Clin. Microbiol. 25: 2407– 2409.

23. Chen, C. K. C.,, R. G. Duford,, H. S. Reynolds,, and J. J. Zambon. 1989. Eikenella corrodens in the human oral cavity. J. Periodontal. 60: 611– 616.

24. Cheng, A. F.,, J. R. South,, and G. L. French. 1988. Eikenella corrodens as a cause of brain abscess. Scand. J. Infect. Dis. 20: 667– 671.

25. Claesson, B.,, E. Falsen,, and B. Kjellman. 1985. Kingella kingae infections: a review and a presentation of data from 10 Swedish cases. Scand. J. Infect. Dis. 17: 233– 243.

26. Cooperman, E. W.,, and A. H. Friedman. 1975. Exogenous Moraxella liquefaciens endophthalmitis. Ophthalmologica 171: 177– 180.

27. Dalrymple, B.,, and J. S. Mattick. 1987. An analysis of the organization and evolution of type 4 fimbrial (MePhe) subunit proteins. J. Mol. Evol. 25: 261– 269.

28. de Groot, R.,, D. Glover,, C. Clausen,, A. L. Smith,, and C. R. Wilson. 1988. Bone and joint infections caused by Kingella kingae: six cases and review of the literature. Rev. Infect. Dis. 10: 998– 1004.

29. Dewhirst, F. E.,, C. K. C. Chen,, B. J. Paster,, and J. J. Zambon. 1993. Phylogeny of species in the family Neisseriaceae isolated from human dental plaque and description of Kingella orale sp. nov. Int. J. Syst. Bacteriol. 43: 490– 499.

30. Dewhirst, F. E.,, B. J. Paster,, S. LaFontaine,, and J. Rood. 1990. Transfer of Kingella indologenes (Snell and Lapage 1976) to the genus Suttonella gen. nov. as Suttonella indologenes comb, nov.; transfer of Bacteroides nodosus (Beveridge 1941) to the genus Dichelobacter gen. nov. as Dichelobacter nodosus comb, nov.; and assignment of the genera Cardiobacterium, Dichelobacter, and Suttonella to Cardiobacteriaceae fam. nov. in the gamma division of Proteobacteria on the basis of 16S rRNA sequence comparisons. Int. J. Syst. Bacteriol. 40: 426– 433.

31. Donnenberg, M. S.,, J. A. Giron,, J. P. Nataro,, and J. B. Kaper. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6: 3427– 3437.

32. Dupon, M.,, C. d'lvernois,, M. Malou,, P. Tauzin-Fin,, F. Boineau,, and J. Y. Lacut. 1991. Sacro-iliac joint infection caused by Eikenella corrodens. Eur. J. Clin. Microbiol. Infect. Dis. 10: 529– 530.

33. Ebright, J. R.,, J. R. Lentino,, and E. Juni. 1982. Endophthalmitis caused by Moraxella nonliquefaciens. Am. J. Clin. Pathol. 77: 362– 363.

34. Eiken, M. 1958. Studies on an anaerobic, rod-shaped gram-negative microorganism: Bacteroides corrodens n. sp. Acta Pathol. Microbiol. Scand. 43: 404– 416.

35. Elleman, T. C.,, and P. A. Hoyne. 1984. Nucleotide sequence of the gene encoding pilin of Bacteroides nodosus, the causal organism of ovine footrot. J. Bacteriol. 160: 1184– 1187.

36. Elleman, T. C.,, P. A. Hoyne,, and A. W. D. Lepper. 1990. Characterization of the pilin gene of Moraxella bovis Dalton 2d and expression of pili from M. bovis in Pseudomonas aeruginosa. Infect. Immun. 58: 1678– 1684.

37. Elleman, T. C.,, P. A. Hoyne,, D. J. Stewart,, N. M. McKern,, and J. E. Peterson. 1986. Expression of pili from Bacteroides nodosus in Pseudomonas aeruginosa. J. Bacteriol. 168: 574– 580.

38. Farley, H.,, I. O. Kliewer,, C. C. Pearson,, and L. E. Foote. 1950. Infectious keratitis of cattle—a preliminary report. Am. J. Vet. Res. 11: 17– 21.

39. Fedukowicz, H.,, M. Alterman,, and R. Newman,. 1971. Two decades of experience with Moraxella. In M. P. Solanes (ed.), XXI International Congress of Ophthalmology. Mexico, 1970. Excerpta Medica, Amsterdam.

40. Fedukowicz, H.,, and H. Horwich. 1953. The gram-negative diplobacillus in hypopyon keratitis. Arch. Ophthalmol. 49: 202– 211.

41. Feldman, S. R.,, and M. J. Petersen. 1989. Botryomycosis caused by Moraxella nonliquefaciens. Cutis 43: 140– 142.

42. Froholm, L. O.,, and K. Bovre,. 1973. The fimbriated state and competence in genetic transformation of three Moraxella species, p. 125– 139. In L. J. Archer (ed.), Bacterial Transformation. Academic Press, Inc., New York..

43. Froholm, L. O.,, and K. Sletten. 1977. Purification and N-terminal sequence of a fimbrial protein from Moraxelta nonliquefaciens. FEBS Lett. 73: 29– 32.

44. Fulks, K. A.,, S. P. Stevens,, M. R. Green,, and C. F. Marrs. 1990. Sequence analysis of the inversion region containing the pilin genes of Moraxella bovis. J. Bacteriol. 172: 310– 316.

45. George, L. W. 1984. Clinical infectious bovine keratoconjunctivitis. Comp. Cont. Ed. Pract. Vet. 6: 712– 724.

46. Geraci, J. E.,, and W. R. Wilson. 1982. Endocarditis due to gram-negative bacteria. Report of 56 cases. Mayo Clin. Proc. 57: 145– 148.

47. Gil-Turnes, C.,, and G. A. Ribelro. 1985. Moraxella bovis hemagglutinins: effect of carbohydrates, heating and erythrocytes. Can. J. Comp. Med. 49: 112– 114.

48. Giron, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710– 713.

49. Glasgow, A. C. (Emory University). Personal communication.

50. Glasgow, A. C.,, K. T. Hughes,, and M. I. Simon,. 1989. Bacterial DNA inversion systems, p. 637– 659. In D. E. Berg, and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C..

51. Goldman, I. S.,, P. D. Ellner,, E. L. Francke,, G. J. Garvey,, H. C. Neu,, and N. Squilla. 1980. Infective endocarditis due to Kingella denitrificans. Ann. Intern. Med. 93: 152– 153.

52. Grayson, M. 1983. Diseases of the Cornea, 2nd ed., p. 122– 123. C. V. Mosby Co., St. Louis.

53. Hackel, M. A.,, F. W. Rosza,, and C. F. Marrs. Submitted for publication.

54. Hackel, M. A. M. 1993. Genetic analysis of Moraxella bovis pilus expression. Ph.D. thesis. University of Michigan, Ann Arbor.

55. Henrichsen, J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36: 478– 503.

56. Henrichsen, J. 1975. The occurrence of twitching motility among gram-negative bacteria. Acta Pathol. Microbiol. Scand. Sect. B 83: 171– 178.

57. Henrichsen, J. 1975. The influence of changes in the environment on twitching motility. Acta Pathol. Microbiol. Scand. Sect. B 83: 179– 186.

58. Henrichsen, J. 1983. Twitching motility. Annu. Rev. Microbiol. 37: 81– 93.

59. Henrichsen, J.,, L. O. Froholm,, and K. Bovre. 1972. Studies on bacterial surface translocation. 2. Correlation of twitching motility and fimbriation in colony variants of Moraxella nonliquefaciens, M. bovis, and M. kingii. Acta Pathol. Microbiol. Scand. Sect. B 80: 445– 452.

60. Henriksen, S. D. 1958. Moraxella duplex var. nonliquefaciens, habitat and antibiotic sensitivity. Acta Pathol. Microbiol. Scand. 43: 157– 161.

61. Henriksen, S. D. 1969. Corroding bacteria from the respiratory tract. I. Moraxella kingii. Acta Pathol. Microbiol. Scand. 75: 85– 90.

62. Henriksen, S. D. 1969. Corroding bacteria from the respiratory tract. II. Bacteroides corrodens. Acta Pathol. Microbiol. Scand. 75: 91– 96.

63. Henriksen, S. D.,, and K. Bovre. 1968. Moraxella kingii sp. nov., a haemolytic, saccharolytic species of the genus Moraxella. J. Gen. Microbiol. 51: 377– 385.

64. Henriksen, S. D.,, and K. Bovre. 1969. Corroding and spreading colonies in Moraxella nonliquefaciens. Acta Pathol. Microbiol. Scand. 76: 459– 463.

65. Henriksen, S. D.,, and K. Bovre. 1976. Transfer of Moraxella kingae Henriksen and Bovre to the genus Kingella gen. nov. in the family Neisseriaceae. Int. J. Syst. Bacteriol. 26: 447– 450.

66. Henson, J. B.,, and L. C. Grumbles. 1960. Infectious bovine keratoconjunctivitis. I. Etiology. Am. J. Vet. Res. 21: 761– 766.

67. Hermodson, M. A.,, K. C. S. Chen,, and T. M. Buchanan. 1978. Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid. Biochemistry 17: 442– 445.

68. Hobbs, M.,, B. Dalrymple,, P. T. Cox,, S. P. Livingstone,, S. F. Delaney,, and J. S. Mattick. 1991. Organization of the fimbrial gene region of Bacteroides nodosus: class I and class II strains. Mol. Microbiol. 5: 543– 560.

69. Hollis, D. G.,, G. L. Wiggins,, and R. E. Weaver. 1972. An unclassified gram-negative rod isolated from the pharynx on Thyer-Martin medium (selective agar). Appl. Microbiol. 24: 772– 777.

70. Jackman, S. H.,, and R. F. Rosenbusch. 1984. In vitro adherence of Moraxella bovis to intact corneal epithelium. Curr. Eye Res. 9: 1107– 1112.

71. Jackson, F. L.,, and Y. Goodman. 1972. Transfer of the facultatively anaerobic organism Bacteroides corrodens Eiken to a new genus Eikenella. Int. J. Syst. Bacteriol. 22: 73– 77.

72. Jayappa, H. G.,, and C. Lehr. 1986. Pathogenicity and immunogenicity of piliated and non-piliated phases of Moraxella bovis in calves. Am. J. Vet. Res. 47: 2217– 2221.

73. Johnson, D. A.,, U. H. Behling,, C.-H. Lai,, M. Listgarten,, S. Socransky,, and A. Nowotny. 1978. Role of bacterial products in periodontitis: immune response in gnotobiotic rats monoinfected with Eikenella corrodens. I nfect. Immun. 19: 246– 253.

74. Johnson, D. A.,, U. H. Behling,, M. Listgarten,, and A. Nowotny. 1978. Role of bacterial products in periodontitis: humoral immune response to Eikenella corrodens. Infect. Immun. 22: 382– 386.

75. Jones, B. R.,, B. E. Andrews,, W. G. Henderson,, and P. B. Schofield. 1957. The patterns of conjunctivitis at Moorfields during 1956. Trans. Ophthalmol. Soc. U.K. 77: 291– 305.

76. Juni, E.,, G. A. Heym,, M. J. Maurer,, and M. L. Miller. 1987. Combined genetic transformation and nutritional assay for identification of Moraxella nonliquefaciens. J. Clin. Microbiol. 25: 1691– 1694.

77. Juni, E.,, G. A. Heym,, and R. D. Newcomb. 1988. Identification of Moraxella bovis by qualitative genetic transformation and nutritional assays. Appl. Environ. Microbiol. 54: 1304– 1306.

78. Kowalski, R. P.,, and J. C. Harwick. 1986. Incidence of Moraxella conjunctival infection. Am. J. Ophthalmol. 101: 437– 440.

78a.. Lautrop, H. 1961. Bacterium anitratum transferred to the genus Cytophaga. Int. Bull. Bacteriol. Nomencl. 11: 107– 108.

79. Lehr, C.,, H. G. Jayappa,, and R. A. Goodnow. 1985. Serologic and protective characterization of Moraxella bovis pili. Cornell Vet. 75: 484– 492.

80. Lepper, A. W. D.,, and L. R. Hermans. 1986. Characterization and quantitation of pilus antigens of Moraxella bovis by ELISA. Aust. Vet. J. 63: 401– 405.

81. Lepper, A. W. D.,, and B. E. Power. 1988. Infectivity and virulence of Australian strains of Moraxella bovis for the murine and bovine eye in relation to pilus serogroup sub-unit size and degree of piliation. Aust. Vet. J. 65: 305– 309.

82. Lobue, T. D.,, T. A. Deutsch,, and R. M. Stein. 1985. Moraxella nonliquefaciens endophthalmitis after trabeculectomy. Am. J. Ophthalmol. 99: 343– 345.

83. Marrs, C. F.,, K. A. Fulks,, M. Hackel,, F. W. Rozsa,, W. W. Ruehl,, S. P. Stevens,, and S. K. Weir,. 1990. Studies on bacterial type 4 pili in the family Neisseriaceae, p. 69– 75. In O. Olsvik, and G. Bukholm (ed.), Applications of Molecular Biology in Diagnosis of Infectious Diseases. Norwegian College of Veterinary Medicine, Oslo.

84. Marrs, C. F.,, F. W. Rozsa,, M. Hackel,, S. P. Stevens,, and A. C. Glasgow. 1990. Identification, cloning and sequencing of piv, a new gene involved in inverting the pilin genes of Moraxella lacunata. J. Bacteriol. 172: 4370– 4377.

85. Marrs, C. F.,, W. W. Ruehl,, G. K. Schoolnik,, and S. Falkow. 1988. Pilin gene phase variation of Moraxella bovis is caused by an inversion of the pilin genes. J. Bacteriol. 170: 3032– 3039.

86. Marrs, C. F.,, G. Schoolnik,, J. M. Koomey,, J. Hardy,, J. Rothbard,, and S. Falkow. 1985. Cloning and sequencing of a Moraxella bovis pilin gene. J. Bacteriol. 163: 132– 139.

87. Mattick, J. S.,, M. M. Bills,, B. J. Anderson,, B. Dalrymple,, M. R. Mott,, and J. R. Egerton. 1987. Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J. Bacteriol. 169: 33– 41.

88. McKern, N. M.,, I. J. O'Donnell,, A. S. Inglis,, D. J. Stewart,, and B. L. Clark. 1983. Amino acid sequence of pilin from Bacteroides nodosus (strain 198), the causative organism of ovine footrot. FEBS Lett. 164: 149– 153.

89. Meyer, T. F.,, E. Billyard,, R. Haas,, S. Storzbach,, and M. So. 1984. Pilus genes of Neisseria gonorrhoeae: chromosomal organization and DNA sequence. Proc. Natl. Acad. Sci. LISA 81: 6110– 6114.

90. Miller, R. B.,, and W. H. Fales. 1984. Infectious bovine keratoconjunctivitis: an update. Vet. Clin. North Am. (Large Anim. Pract.) 6: 597– 608.

91. Mitsui, Y.,, S. Hinokuma,, and C. Tanaka. 1951. Etiology of angular conjunctivitis. Am. J. Ophthalmol. 34: 1579– 1586.

92. Moore, L. J.,, and J. M. Rutter. 1987. Antigenic analysis of fimbrial proteins from Moraxella bovis. J. Clin. Microbiol. 25: 2063– 2070.

93. Morrison, V. A.,, and K. F. Wagner. 1989. Clinical manifestations of Kingella kingae infections: case report and review. Rev. Infect. Dis. 11: 776– 782.

94. Pasloske, B. L.,, B. B. Finlay,, and W. Paranchych. 1985. Cloning and sequencing of the Pseudomonas aeruginosa PAK pilin gene. FEBS Lett. 183: 408– 412.

95. Patel, N. J.,, T. L. Moore,, T. D. Weiss,, and J. Zuckner. 1983. Kingella kingae infectious arthritis: case report and review of literature of Kingella and Moraxella infections. Arthritis Rheum. 26: 557– 559.

96. Patel, P.,, C. F. Marrs,, J. S. Mattick,, W. W. Ruehl,, R. K. Taylor,, and M. Koomey. 1991. Shared antigenicity and immunogenicity of type 4 pilins expressed by Pseudomonas aeruginosa, Moraxella bovis, Neisseria gonorrhoeae, Dichelobacter nodosus, and Vibrio cholerae. Infect. Immun. 59: 4674– 4676.

97. Pedersen, K. B. 1970. Moraxella bovis isolated from cattle with infectious keratoconjunctivitis. Acta Pathol. Microbiol. Scand. Sect. B 78: 429– 434.

98. Pedersen, K. B.,, L. O. Froholm,, and K. Bovre. 1972. Fimbriation and colony type of Moraxella bovis in relation to conjunctival colonization and development of keratoconjunctivitis in cattle. Acta Pathol. Microbiol. Scand. Sect. B 80: 911– 918.

99. Perez-Pomata, M. T.,, J. Dominguez,, P. Horcajo,, F. Santidrian,, and J. Bisquert. 1992. Spleen abscess caused by Eikenella corrodens. Eur. J. Clin. Microbiol. Infect. Dis. 11: 162– 163.

100. Piechaud, M. 1963. Motility in the genus Moraxella. Ann. Inst. Pasteur 104: 291– 297.

101. Pollner, J. H.,, A. Khan,, and C. U. Tuazon. 1992. Severe soft-tissue infection caused by Eikenella corrodens. Clin. Infect. Dis. 15: 740– 741.

102. Pugh, G. W.,, and D. E. Hughes. 1970. Inhibition of autoagglutination of Moraxella bovis by 10% MgCl 2. Appl. Microbiol. 19: 201– 203.

103.. Pugh, G. W.,, and D. E. Hughes. 1971. Infectious bovine keratoconjunctivitis induced by different experimental methods. Cornell Vet. 61: 23– 45.

104. Pugh, G. W.,, and D. E. Hughes. 1972. Bovine infectious keratoconjunctivitis: Moraxella bovis as the sole etiologic agent in a winter epizootic. J. Am. Vet. Med. Assoc. 161: 481– 486.

105. Pugh, G. W.,, and D. E. Hughes. 1975. Bovine infectious keratoconjunctivitis: carrier state of Moraxella bovis and the development of preventive measures against disease. J. Am. Vet. Med. Assoc. 167: 310– 313.

106. Pugh, G. W.,, and D. E. Hughes. 1976. Experimental production of infectious bovine keratoconjunctivitis: comparison of serological and immunological responses using pili fractions of Moraxella bovis. Can. J. Comp. Med. 40: 60– 66.

107. Pugh, G. W.,, D. E. Hughes,, and G. D. Booth. 1977. Experimentally induced infectious bovine keratoconjunctivitis: effectiveness of a pilus vaccine against exposure to homologous strains of Moraxella bovis. Am. J. Vet. Res. 38: 1519– 1522.

108. Pugh, G. W.,, D. E. Hughes,, V. D. Schulz,, and C. K. Graham. 1976. Experimentally induced infectious bovine keratoconjunctivitis: resistance of vaccinated cattle to homologous and heterologous strains of Moraxella bovis. Am. J. Vet. Res. 37: 57– 60.

109. Pugh, G. W.,, T. J. McDonald,, and A. B. Larsen. 1978. Experimentally induced infectious bovine keratoconjunctivitis: potentiation of a Moraxella bovis pilus vaccine immunogenicity by vaccination with Mycobacterium paratuberculosis bacterin. Am. J. Vet. Res. 39: 1656– 1661.

110. Raffensperger, J. G. 1986. Eikenella corrodens infections in children. J. Pediatr. Surg. 21: 644– 646.

111. Rao, V. K.,, and A. Progulske-Fox. 1993. Cloning and sequencing of two type 4 (N-methylphenylalanine) pilin genes from Eikenella corrodens. J. Gen. Microbiol. 139: 651– 660.

112. Rao, V. K.,, J. A. Whitlock,, and A. Progulske-Fox. 1993. Cloning, characterization and sequencing of two haemagglutinin genes from Eikenella corrodens. J. Gen. Microbiol. 139: 639– 650.

113. Ringvold, A.,, E. Vik,, and L. S. Bevanger. 1985. Moraxella lacunata isolated from epidemic conjunctivitis among teen-aged females. Acta Ophthalmol. 63: 427– 431.

114. Rosett, W.,, D. M. Heck,, and G. R. Hodges. 1976. Pneumonitis and pulmonary abscess associated with Moraxella nonliquefaciens. Chest 70: 664– 665.

115. Rossau, R.,, A. van Lanschoot,, M. Gillis,, and J. DeLey. 1991. Taxonomy of Moraxellaceae fam. nov., a new bacterial family to accommodate the genera Moraxella, Acinetobacter, and Psychrobacter and related organisms. Int. J. Syst. Bacteriol. 41: 310– 319.

116. Rozsa, F. W.,, M. Hackel,, S. P. Stevens,, and C. F. Marrs,. 1991. Analysis of the pilin gene inversion region of Moraxella lacunata, p. 475– 480. In M. Achtman,, P. Kohl,, C. Marchal,, G. Morelli,, A. Seiler,, and B. Thiesen (ed.), Neisseria 1990. Walter de Gruyter & Co., Berlin.

117. Rozsa, F. W.,, and C. F. Marrs. 1991. Interesting sequence differences between the pilin gene inversion regions of Moraxella lacunata ATCC 17956 and Moraxella bovis Epp63. J. Bacteriol. 173: 4000– 4006.

118. Ruehl, W. W.,, C. F. Marrs,, M. K. Beard,, V. Shokooki,, J. R. Hinojoza,, S. Banks,, D. Bieber,, and J. S. Mattick. 1993. Q pili enhance the attachment of Moraxella bovis to bovine corneas in vitro. Mol. Microbiol. 7: 285– 288.

119. Ruehl, W. W.,, C. F. Marrs,, R. Fernandez,, S. Falkow,, and G. K. Schoolnik. 1988. Purification, characterization, and pathogenicity of Moraxella bovis pili. J. Exp. Med. 168: 983– 1002.

120. Ruehl, W. W.,, C. F. Marrs,, L. George,, S. J. M. Banks,, and G. K. Schoolnik. 1993. Infection rates, disease frequency, pilin gene rearrangement, and pilin expression in calves inoculated with Moraxella bovis pilin specific isogenic variants. Am. J. Vet. Res. 54: 248– 253.

121. Samejima, Y.,, S. Ebisu,, and H. Okada. 1990. Effect of infection with Eikenella corrodens on the progression of ligature-induced periodontitis in rats. J. Periodontal Res. 25: 308– 315.

122. Sandhu, T. S.,, F. H. White,, and C. F. Simpson. 1974. Association of pili with rough colony type of Moraxella bovis. Am. J. Vet. Res. 35: 437– 439.

123. Sanyal, S. K.,, N. Wilson,, K. Twum-Danso,, A. Abomelha,, and S. Sohel. 1990. Moraxella endocarditis following balloon angioplasty of aortic coarctation. Am. Heart J. 119: 1421– 1423.

124. Sastry, P. A.,, B. B. Finlay,, B. L. Pasloske,, W. Paranchych,, J. R. Pearlstone,, and L. B. Smillie. 1985. Comparative studies of the amino acid and nucleotide sequences of pilin derived from Pseudomonas aeruginosa PAK and PAO. J. Bacteriol. 164: 571– 577.

125. Sharma, D. L. B. 1974. Fatal septicaemia due to Moraxella nonliquefaciens. Arch. Dis. Child. 49: 966– 967.

126. Silberfarb, P. M.,, and J. E. Lawe. 1968. Endocarditis due to Moraxella liquefaciens. Arch. Intern. Med. 122: 512– 513.

127. Simpson, C. F.,, F. H. White,, and T. S. Sandhu. 1976. The structure of pili (fimbriae) of Moraxella bovis. Can. J. Comp. Med. 40: 1– 4.

128. Slatter, D. H.,, M. E. Edwards,, C. D. Hawkins,, and G. E. Wilcox. 1982. A national survey of the occurrence of infectious bovine keratoconjunctivitis. Aust. Vet. J. 59: 65– 68.

129. Slatter, D. H.,, M. E. Edwards,, C. D. Hawkins,, and G. E. Wilcox. 1982. A national survey of the clinical features, treatment and importance of infectious bovine keratoconjunctivitis. Aust. Vet. J. 59: 69– 72.

130. Snell, J. J. S.,, and S. Lapage. 1976. Transfer of some saccharolytic Moraxella species to Kingella Henriksen and Bovre 1976, with descriptions of Kingella indologenes sp. nov. and Kingella denitrificans sp. nov. Int. J. Syst. Bacteriol. 26: 451– 458.

131. Stein, A.,, N. Teysseire,, C. Capobianco,, R. Bricot,, and D. Raoult. 1993. Eikenella corrodens, a rare cause of pancreatic abscess: two case reports and review. Clin. Infect. Dis. 17: 273– 275.

132. Strom, M. S.,, and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47: 565– 596.

133. Swann, R. A.,, and B. Holmes. 1984. Infective endocarditis caused by Kingella denitrificans. J. Clin. Pathol. 37: 1384– 1387.

134. Tami, T. A.,, and G. S. Parker. 1984. Eikenella corrodens: an emerging pathogen in head and neck infections. Arch. Otolaryngol. 110: 752– 754.

135. Tanner, A. C. R.,, C. Haffer,, G. T. Brathal,, R. A. Visconti,, and S. S. Socransky. 1979. A study of the bacteria associated with advancing periodontitis in man. J. Clin. Periodontal. 6: 278– 307.

136. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 81: 2833– 2837.

137. Thygeson, P.,, and S. J. Kimura. 1963. Chronic conjunctivitis. Trans. Am. Acad. Ophthalmol. Otolaryngol. 67: 494– 517.

138. Tonjum, T.,, G. Bukholm,, and K. Bovre. 1989. Differentiation of some species of Neisseriaceae and other bacterial groups by DNA-DNA hybridization. APMIS 97: 395– 405.

139. Tonjum, T.,, D. A. Caugant,, and K. Bovre. 1992. Differentiation of Moraxella nonliquefaciens, M. lacunata, and M. bovis by using mutilocus enzyme electrophoresis and hybridization with pilin-specific DNA probes. J. Clin. Microbiol. 30: 3099– 3107.

140. Tonjum, T.,, N. Hagen,, and K. Bovre. 1985. Identification of Eikenella corrodens and Cardiobacterium hominis by genetic transformation. Acta. Pathol. Microbiol. Immunol. Scand. Sect. B 93: 389– 394.

141. Tonjum, T.,, C. F. Marrs,, F. W. Rozsa,, and K. Bovre. 1991. The type 4 pilin of Moraxella nonliquefaciens exhibits unique similarities with the pilins of Neisseria gonorrhoeae and Dichelobacter (Bacteriodes) nodosus. J. Gen. Microbiol. 137: 2483– 2490.

142. Tonjum, T.,, S. Weir,, K. Bovre,, V. K. Rao,, A. Progulske-Fox,, and C. Marrs. 1993. Sequence divergence in two tandemly located pilin genes of Eikenella corrodens. Infect. Immun. 61: 1909– 1916.

143. Toshniwal, R.,, T. C. Draghi,, F. E. Kocka,, and C. A. Kallick. 1986. Manifestations of Kingella kingae infections in adults: resemblance to neisserial infections. Diagn. Microbiol. Infect. Dis. 5: 81– 85.

144. van Bjjsterveld, O. P. 1967. Acute conjunctivitis and Moraxella. Am. J. Ophthalmol. 63: 1702– 1705.

145. van Bijsterveld, O. P. 1971. In-vitro phagocytosis in pyridoxine deficiency. J. Med. Microbiol. 4: 165– 170.

146. van Bijsterveld, O. P. 1972. The incidence of Moraxella on mucous membranes and the skin. Am. J. Ophthalmol. 14: 11– 1$.

147. van Bijsterveid, O. P. 1973. Host-parasite relationship and taxonomic position of Moraxella and morphologically related organisms. Am. J. Ophthalmol. 76: 545– 554.

148. Vandergaast, N.,, and R. F. Rosenbusch. 1989. Infectious bovine keratoconjunctivitis epizootic associated with area-wide emergence of a new Moraxella bovis pilus type. Am. J. Vet. Res. 50: 1437– 1441.

149. Verbruggen, A.-M.,, D. Hauglustaine,, F. Schildermans,, L. van der Hauwaert,, J. J. Rombouts,, G. Wauters,, and J. Vandepitte. 1986. Infections caused by Kingella kingae: report of four cases and review. J. Infect. 13: 133– 142.

150. Webber, J. J.,, and L. A. Selby. 1981. Risk factors related to the prevalence of infectious bovine keratoconjunctivitis. J. Am. Vet. Med. Assoc. 179: 823– 826.

151. Weir, S. 1993. Studies of pili in Branhamella catarrhalis, Eikenella corrodens, and Kingella denitrificans. Ph.D. thesis. University of Michigan, Ann Arbor..

152. Weir, S. K.,, and C. F. Marrs. 1992. Identification of type 4 pili in Kingella denitrificans. Infect. Immun. 60: 3437– 3441.