Campylobacter fetus comprises two subspecies, C. fetus subsp. fetus and C. fetus subsp. venerealis, which are considered emerging pathogens in humans and animals. Comparisons at the genome level have revealed modest subspecies-specific variation; nevertheless, these two subspecies show distinct host and niche preferences. C. fetus subsp. fetus is a commensal and pathogen of domesticated animals that can be transmitted to humans via contaminated food. The clinical features of human infection can be severe, especially in impaired hosts. In contrast, C. fetus subsp. venerealis is a sexually transmitted pathogen essentially restricted to cattle. Infections leading to bovine venereal campylobacteriosis cause substantial economic losses due to abortion and infertility. Recent genome sequencing of the two subspecies has advanced our understanding of C. fetus adaptations through comparative genomics and the identification of subspecies-specific gene regions predicted to be involved in pathogenesis. The most striking difference between the subspecies is the highly subspecies-specific association of a pathogenicity island in the C. fetus subsp. venerealis chromosome. The inserted region encodes a Type 4 secretion system, which contributes to virulence properties of this organism in vitro. This review describes the main differences in epidemiological, phenotypic, and molecular characteristics of the two subspecies and summarizes recent advances towards understanding the molecular mechanisms of C. fetus pathogenesis.
1. B.M. Allos 2001 Campylobacter jejuni infections: update on emerging issues and trends Clin Infect Dis 32 1201–1206.
2. A.J. Lastovica B.M. Allos 2008 Clinical significance of Campylobacter and related species other than Campylobacter jejuni and Campylobacter coli. I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC 123–149.
3. P.S. Mead L. Slutsker V. Dietz L.F. Mccaig J.S. Bresee C. Shapiro P.M. Griffin R.V. Tauxe 1999 Food-related illness and death in the United States Emerg Infect Dis 5 607–625.
4. M.J. Blaser 1998 Campylobacter fetus — emerging infection and model system for bacterial pathogenesis at mucosal surfaces Clin Infect Dis 27 256–258.
5. M.J. Blaser D.G. Newell S.A. Thompson E.L. Zechner 2008 Pathogenesis of Campylobacter fetus infections I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC 401–428.
6. J.L. Penner 1988 The genus Campylobacter: a decade of progress Clin Microbiol Rev 1 157–172.
7. M.B. Skirrow J. Benjamin 1980 ’1001’ Campylobacters: cultural characteristics of intestinal campylobacters from man and animals J Hyg (Lond) 85 427–442.
8. C.M. Logue J.S. Sherwood L.M. Elijah P.A. Olah M.R. Dockter 2003 The incidence of Campylobacter spp. on processed turkey from processing plants in the midwestern United States J Appl Microbiol 95 234–241.
9. S. Harvey J.R. Greenwood 1985 Isolation of Campylobacter fetus from a pet turtle J Clin Microbiol 21 260–261.
10. R.P. Rennie D. Strong D.E. Taylor S.M. Salama C. Davidson H. Tabor 1994 Campylobacter fetus diarrhea in a Hutterite colony: epidemiological observations and typing of the causative organism J Clin Microbiol 32 721–724.
11. B.S. Klein J.M. Vergeront M.J. Blaser P. Edmonds D.J. Brenner D. Janssen J.P. Davis 1986 Campylobacter infection associated with raw milk. An outbreak of gastroenteritis due to Campylobacter jejuni and thermotolerant Campylobacter fetus subsp fetus JAMA 255 361–364.
12. S. Ichiyama S. Hirai T. Minami Y. Nishiyama S. Shimizu K. Shimokata M. Ohta 1998 Campylobacter fetus subspecies fetus cellulitis associated with bacteremia in debilitated hosts Clin Infect Dis 27 252–255.
13. K. Miki R. Maekura T. Hiraga A. Hirotani H. Hashimoto S. Kitada M. Miki K. Yoshimura N. Naka M. Motone T. Fujikawa S. Takashima R. Kitazume H. Kanzaki S. Nakatani H. Watanuki O. Tagusari J. Kobayashi M. Ito 2005 Infective tricuspid valve endocarditis with pulmonary emboli caused by Campylobacter fetus after tooth extraction Intern Med 44 1055–1059.
14. M.B. Skirrow D.M. Jones E. Sutcliffe J. Benjamin 1993 Campylobacter bacteraemia in England and Wales, 1981–91 Epidemiol Infect 110 567–573.
15. C. Pigrau R. Bartolome B. Almirante A.M. Planes J. Gavalda A. Pahissa 1997 Bacteremia due to Campylobacter species: clinical findings and antimicrobial susceptibility patterns Clin Infect Dis 25 1414–1420.
16. G. Anstead J. Jorgensen F. Craig M. Blaser T. Patterson 2001 Thermophilic multidrug-resistant Campylobacter fetus infection with hypersplenism and histiocytic phagocytosis in a patient with acquired immunodeficiency syndrome Clin Infect Dis 32 295–296.
17. J. Pacanowski V. Lalande K. Lacombe C. Boudraa P. Lesprit P. Legrand D. Trystram N. Kassis G. Arlet J.L. Mainardi F. Doucet-Populaire P.M. Girard J.L. Meynard 2008 Campylobacter bacteremia: clinical features and factors associated with fatal outcome Clin Infect Dis 47 790–796.
18. C. Tremblay C. Gaudreau M. Lorange 2003 Epidemiology and antimicrobial susceptibilities of 111 Campylobacter fetus subsp. fetus strains isolated in Quebec, Canada, from 1983 to 2000 J Clin Microbiol 41 463–466.
19. L. Gazaigne P. Legrand B. Renaud B. Bourra E. Taillandier C. Brun-Buisson P. Lesprit 2008 Campylobacter fetus bloodstream infection: risk factors and clinical features Eur J Clin Microbiol Infect Dis 27 185–189.
20. S.S. Kanj G.F. Araj A. Taher L.B. Reller 2001 Campylobacter fetus pericarditis in a patient with beta-thalassemia: case report and review of the literature Clin Microbiol Infect 7 510–513.
21. F. Dronda I. Garcia-Arata E. Navas L. De Rafael 1998 Meningitis in adults due to Campylobacter fetus subspecies fetus Clin Infect Dis 27 906–907.
22. G.E. Steinkraus B.D. Wright 1994 Septic abortion with intact fetal membranes caused by Campylobacter fetus subsp. fetus J Clin Microbiol 32 1608–1609.
23. R.M. Smibert 1978 The genus Campylobacter Annu Rev Microbiol 32 673–709.
24. M.A. Van Bergen S. Linnane J.P. Van Putten J.A. Wagenaar 2005 Global detection and identification of Campylobacter fetus subsp. venerealis Rev Sci Tech 24 1017–1026.
25. G.I. Perez-Perez M.J. Blaser J.H. Bryner 1986 Lipopolysaccharide structures of Campylobacter fetus are related to heat-stable serogroups Infect Immun 51 209–212.
26. A.P. Moran D.T. O'malley T.U. Kosunen I.M. Helander 1994 Biochemical characterization of Campylobacter fetus lipopolysaccharides Infect Immun 62 3922–3929.
27. L.Y. Yang Z.H. Pei S. Fujimoto M.J. Blaser 1992 Reattachment of surface array proteins to Campylobacter fetus cells J Bacteriol 174 1258–1267.
28. Z.C. Tu F.E. Dewhirst M.J. Blaser 2001 Evidence that the Campylobacter fetus sap locus is an ancient genomic constituent with origins before mammals and reptiles diverged Infect Immun 69 2237–2244.
29. M.A. Van Bergen K.E. Dingle M.C. Maiden D.G. Newell L. Van Der Graaf-Van Bloois J.P. Van Putten J.A. Wagenaar 2005 Clonal nature of Campylobacter fetus as defined by multilocus sequence typing J Clin Microbiol 43 5888–5898.
30. Z.C. Tu W. Eisner B.N. Kreiswirth M.J. Blaser 2005 Genetic divergence of Campylobacter fetus strains of mammal and reptile origins J Clin Microbiol 43 3334–3340.
31. Gilbert MJ , Miller WG, Yee E, Duim B, Wagenaar JA (2011): Whole genome sequencing of Campylobacter sp. found in reptiles, CHRO 2011 poster A420, Vancouver, Canada.
32. Gilbert MJ , Miller WG, Yee E, Duim B, Lawson AJ, Blaser MJ, Wagenaar JA (2011): Whole genome sequencing for taxonomic positioning of reptilian Campylobacter fetus, CHRO 2011 poster A421, Vancouver, Canada.
33. M.A. Van Bergen J.P.M. Van Putten K.E. Dingle M.J. Blaser J.A. Wagenaar 2008 Isolation, identification, subspecies differentiation, and typing of Campylobacter fetus I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC 213–225.
34. S.M. Man 2011 The clinical importance of emerging Campylobacter species Nat Rev Gastroenterol Hepatol 8 669–685.
35. W.L. Wang M.J. Blaser 1986 Detection of pathogenic Campylobacter species in blood culture systems J Clin Microbiol 23 709–714.
36. H.J. Monke B.C. Love T.E. Wittum D.R. Monke B.A. Byrum 2002 Effect of transport enrichment medium, transport time, and growth medium on the detection of Campylobacter fetus subsp. venerealis J Vet Diagn Invest 14 35–39.
37. J.G. Lecce 1958 Some biochemical characteristics of Vibrio fetus and other related Vibrios isolated from animals J Bacteriol 76 312–316.
38. M. V'eron R. Chatelain 1973 Taxonomic study of the genus Campylobacter Sebald and V'eron and designation of the neotype strain for the type species, Campylobacter fetus (Smith and Taylor) Sebald and V'eron Int J Syst Bacteriol 23 122–134.
39. S. Hum K. Quinn J. Brunner S.L. On 1997 Evaluation of a PCR assay for identification and differentiation of Campylobacter fetus subspecies Aust Vet J 75 827–831.
40. G. Wang C.G. Clark T.M. Taylor C. Pucknell C. Barton L. Price D.L. Woodward F.G. Rodgers 2002 Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus J Clin Microbiol 40 4744–4747.
41. K. Willoughby P.F. Nettleton M. Quirie M.A. Maley G. Foster M. Toszeghy D.G. Newell 2005 A multiplex polymerase chain reaction to detect and differentiate Campylobacter fetus subspecies fetus and Campylobacter fetus -species venerealis: use on UK isolates of C. fetus and other Campylobacter spp J Appl Microbiol 99 758–766.
42. M.A. Van Bergen G. Simons L. Van Der Graaf-Van Bloois J.P. Van Putten J. Rombout I. Wesley J.A. Wagenaar 2005 Amplified fragment length polymorphism based identification of genetic markers and novel PCR assay for differentiation of Campylobacter fetus subspecies J Med Microbiol 54 1217–1224.
43. L. McMillen G. Fordyce V.J. Doogan A.E. Lew 2006 Comparison of culture and a novel 5′ Taq nuclease assay for direct detection of Campylobacter fetus subsp. venerealis in clinical specimens from cattle J Clin Microbiol 44 938–945.
44. F. Schulze A. Bagon W. Muller H. Hotzel 2006 Identification of Campylobacter fetus subspecies by phenotypic differentiation and PCR J Clin Microbiol 44 2019–2024.
45. J.A. Wagenaar M.A. Van Bergen D.G. Newell R. Grogono-Thomas B. Duim 2001 Comparative study using amplified fragment length polymorphism fingerprinting, PCR genotyping, and phenotyping to differentiate Campylobacter fetus strains isolated from animals J Clin Microbiol 39 2283–2286.
46. J. Parkhill B.W. Wren K. Mungall J.M. Ketley C. Churcher D. Basham T. Chillingworth R.M. Davies T. Feltwell S. Holroyd K. Jagels A.V. Karlyshev S. Moule M.J. Pallen C.W. Penn M.A. Quail M.A. Rajandream K.M. Rutherford A.H. Van Vliet S. Whitehead B.G. Barrell 2000 The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences Nature 403 665–668.
47. S.M. Salama M.M. Garcia D.E. Taylor 1992 Differentiation of the subspecies of Campylobacter fetus by genomic sizing Int J Syst Bacteriol 42 446–450.
48. P.M. Moolhuijzen A.E. Lew-Tabor B.M. Wlodek F.G. Aguero D.J. Comerci R.A. Ugalde D.O. Sanchez R. Appels M. Bellgard 2009 Genomic analysis of Campylobacter fetus subspecies: identification of candidate virulence determinants and diagnostic assay targets BMC Microbiol 9 86.
49. A.P. Stynen A.P. Lage R.J. Moore A.M. Rezende V.D. De Resende C. Ruy Pde N. Daher M. Resende Dde S.S. De Almeida C. Soares Sde V.A. De Abreu A.A. Rocha A.R. Dos Santos E.G. Barbosa D.F. Costa F.A. Dorella A. Miyoshi A.R. De Lima F.D. Campos P.G. De Sa T.S. Lopes R.M. Rodrigues A.R. Carneiro T. Leao L.T. Cerdeira R.T. Ramos A. Silva V. Azevedo J.C. Ruiz 2011 Complete genome sequence of type strain Campylobacter fetus subsp. venerealis NCTC 10354T J Bacteriol 193 5871–5872.
50. Van Graaf-Van Bloois L , Miller WG, Yee E, Duim B, Wagenaar, JA (2011): Whole genome sequencing of Campylobacter fetus subspecies, CHRO 2011 poster A434, Vancouver, Canada.
51. G. Gorkiewicz S. Kienesberger C. Schober S.R. Scheicher C. Gully R. Zechner E.L. Zechner 2010 A genomic island defines subspecies-specific virulence features of the host-adapted pathogen Campylobacter fetus subsp. venerealis J Bacteriol 192 502–517.
52. S. Kienesberger G. Gorkiewicz H. Wolinski E.L. Zechner 2011 New molecular microbiology approaches in the study of Campylobacter fetus Microb Biotechnol 4 8–19.
53. Kienesberger S , Sprenger H, Wolfgruber S, Thallinger G, Zechner EL, Gorkiewicz G: Comparative genetic analysis of Campylobacter fetus subspecies: Model system for bacterial niche specificity and mucosal infection. (2012).
54. N. Jarvinen M. Maki J. Rabina C. Roos P. Mattila R. Renkonen 2001 Cloning and expression of Helicobacter pylori GDP-l-fucose synthesizing enzymes (GMD and GMER) in Saccharomyces cerevisiae Eur J Biochem 268 6458–6464.
55. B. Wu Y. Zhang P.G. Wang 2001 Identification and characterization of GDP-d-mannose 4,6-dehydratase and GDP-l-fucose snthetase in a GDP-l-fucose biosynthetic gene cluster from Helicobacter pylori Biochem Biophys Res Commun 285 364–371.
56. C.C. McGowan A. Necheva S.A. Thompson T.L. Cover M.J. Blaser 1998 Acid-induced expression of an LPS-associated gene in Helicobacter pylori Mol Microbiol 30 19–31.
57. R.A. Batchelor B.M. Pearson L.M. Friis P. Guerry J.M. Wells 2004 Nucleotide sequences and comparison of two large conjugative plasmids from different Campylobacter species Microbiology 150 3507–3517.
58. L.M. Friis C. Pin D.E. Taylor B.M. Pearson J.M. Wells 2007 A role for the tet(O) plasmid in maintaining Campylobacter plasticity Plasmid 57 18–28.
59. D. Kersulyte B. Velapatino G. Dailide A.K. Mukhopadhyay Y. Ito L. Cahuayme A.J. Parkinson R.H. Gilman D.E. Berg 2002 Transposable element ISHp608 of Helicobacter pylori: nonrandom geographic distribution, functional organization, and insertion specificity J Bacteriol 184 992–1002.
60. H. Schmidt M. Hensel 2004 Pathogenicity islands in bacterial pathogenesis Clin Microbiol Rev 17 14–56.
61. C. Abril I. Brodard V. Perreten 2010 Two novel antibiotic resistance genes, tet(44) and ant(6)-Ib, are located within a transferable pathogenicity island in Campylobacter fetus subsp. fetus Antimicrob Agents Chemother 54 3052–3055.
62. S. Backert T.F. Meyer 2006 Type IV secretion systems and their effectors in bacterial pathogenesis Curr Opin Microbiol 9 207–217.
63. W. Fischer R. Haas S. Odenbreit 2002 Type IV secretion systems in pathogenic bacteria Int J Med Microbiol 292 159–168.
64. H. Nagai C.R. Roy 2003 Show me the substrates: modulation of host cell function by type IV secretion systems Cell Microbiol 5 373–383.
65. C.E. Alvarez-Martinez P.J. Christie 2009 Biological diversity of prokaryotic type IV secretion systems Microbiol Mol Biol Rev 73 775–808.
66. D.J. Bacon R.A. Alm L. Hu T.E. Hickey C.P. Ewing R.A. Batchelor T.J. Trust P. Guerry 2002 DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81–176 Infect Immun 70 6242–6250.
67. D.J. Bacon R.A. Alm D.H. Burr L. Hu D.J. Kopecko C.P. Ewing T.J. Trust P. Guerry 2000 Involvement of a plasmid in virulence of Campylobacter jejuni 81–176 Infect Immun 68 4384–4390.
68. S. Kienesberger C. Schober Trummler A. Fauster S. Lang H. Sprenger G. Gorkiewicz E.L. Zechner 2011 Interbacterial macromolecular transfer by the Campylobacter fetus subsp. venerealis type IV secretion system J Bacteriol 193 744–758.
69. R. Utsumi Y. Nakamoto M. Kawamukai M. Himeno T. Komano 1982 Involvement of cyclic AMP and its receptor protein in filamentation of an Escherichia coli fic mutant J Bacteriol 151 807–812.
70. C.A. Worby S. Mattoo R.P. Kruger L.B. Corbeil A. Koller J.C. Mendez B. Zekarias C. Lazar J.E. Dixon 2009 The fic domain: regulation of cell signaling by adenylylation Mol Cell 34 93–103.
71. M.L. Yarbrough Y. Li L.N. Kinch N.V. Grishin H.L. Ball K. Orth 2009 AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling Science 323 269–272.
72. X. Pan A. Luhrmann A. Satoh M.A. Laskowski-Arce C.R. Roy 2008 Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors Science 320 1651–1654.
73. M.C. Schmid F. Scheidegger M. Dehio N. Balmelle-Devaux R. Schulein P. Guye C.S. Chennakesava B. Biedermann C. Dehio 2006 A translocated bacterial protein protects vascular endothelial cells from apoptosis PLoS Pathog 2 e115.
74. B. Zekarias S. Mattoo C. Worby J. Lehmann R.F. Rosenbusch L.B. Corbeil 2010 Histophilus somni IbpA DR2/Fic in virulence and immunoprotection at the natural host alveolar epithelial barrier Infect Immun 78 1850–1858.
75. A.C. Vergunst B. Schrammeijer A. Den Dulk-Ras C.M. De Vlaam T.J. Regensburg-Tuink P.J. Hooykaas 2000 VirB/D4-dependent protein translocation from Agrobacterium into plant cells Science 290 979–982.
76. M.P. Sory G.R. Cornelis 1994 Translocation of a hybrid YopEadenylate cyclase from Yersinia enterocolitica into HeLa cells Mol Microbiol 14 583–594.
77. L. Hu D.J. Kopecko 2008 Cell Biology of Human Host Cell Entry by Campylobacter jejuni I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC 297–313.
78. C.L. Larson J.E. Christensen S.A. Pacheco S.A. Minnich M.E. Konkel 2008 Campylobacter jejuni secretes proteins via the flagellar type III secretion system that contribute to host cell invasion and gastroenteritis I. Nachamkin C.M. Szymanski M.J. Blaser Campylobacter 3rd edn ASM Press Washington, DC 315–332.
79. M.E. Konkel S.G. Garvis S.L. Tipton D.E. Anderson Jr. W. Cieplak Jr. 1997 Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campy lo bacter jejuni Mol Microbiol 24 953–963.
80. L.L. Graham 2002 Campylobacter fetus adheres to and enters INT 407 cells Can J Microbiol 48 995–1007.
81. M.E. Konkel L.A. Joens 1989 Adhesion to and invasion of HEp-2 cells by Campylobacter spp Infect Immun 57 2984–2990.
82. L.L. Graham T. Friel R.L. Woodman 2008 Fibronectin enhances Campylobacter fetus interaction with extracellular matrix components and INT 407 cells Can J Microbiol 54 37–47.
83. N.T. Baker L.L. Graham 2010 Campylobacter fetus translocation across Caco-2 cell monolayers Microb Pathog 49 260–272.
84. H.L. Nielsen H. Nielsen T. Ejlertsen J. Engberg D. Gunzel M. Zeitz N.A. Hering M. Fromm J.D. Schulzke R. Bucker 2011 Oral and fecal Campylobacter concisus strains perturb barrier function by apoptosis induction in HT-29/B6 intestinal epithelial cells PLoS One 6 e23858.
85. S.M. Man N.O. Kaakoush S.T. Leach L. Nahidi H.K. Lu J. Norman A.S. Day L. Zhang H.M. Mitchell 2010 Host attachment, invasion, and stimulation of proinflammatory cytokines by Campylobacter concisus and other non-Campylobacter jejuni Campylobacter species J Infect Dis 202 1855–1865.
86. L.B. Van Alphen N.M. Bleumink-Pluym K.D. Rochat B.W. Van Balkom M.M. Wosten J.P. Van Putten 2008 Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells Cell Microbiol 10 53–66.
87. C.L. Pickett E.C. Pesci D.L. Cottle G. Russell A.N. Erdem H. Zeytin 1996 Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene Infect Immun 64 2070–2078.
88. M. Lara-Tejero J.E. Galan 2001 CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity Infect Immun 69 4358–4365.
89. R.B. Lee D.C. Hassane D.L. Cottle C.L. Pickett 2003 Interactions of Campylobacter jejuni cytolethal distending toxin subunits CdtA and CdtC with HeLa cells Infect Immun 71 4883–4890.
90. M. Lara-Tejero J.E. Galan 2000 A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein Science 290 354–357.
91. M. Asakura W. Samosornsuk M. Taguchi K. Kobayashi N. Misawa M. Kusumoto K. Nishimura A. Matsuhisa S. Yamasaki 2007 Comparative analysis of cytolethal distending toxin (cdt) genes among Campylobacter jejuni, C. coli and C. fetus strains Microb Pathog 42 174–183.
92. E.C. McCoy D. Doyle H. Wiltberger K. Burda A.J. Winter 1975 Flagellar ultrastructure and flagella-associated antigens of Campylobacter fetus J Bacteriol 122 307–315.
93. E.C. McCoy D. Doyle K. Burda L.B. Corbeil A.J. Winter 1975 Superficial antigens of Campylobacter (Vibrio) fetus: characterization of antiphagocytic component Infect Immun 11 517–525.
94. M.J. Blaser P.F. Smith P.F. Kohler 1985 Susceptibility of Campylobacter isolates to the bactericidal activity of human serum J Infect Dis 151 227–235.
95. M.J. Blaser P.F. Smith J.A. Hopkins I. Heinzer J.H. Bryner W.L. Wang 1987 Pathogenesis of Campylobacter fetus infections: serum resistance associated with high-molecular-weight surface proteins J Infect Dis 155 696–706.
96. M.J. Blaser P.F. Smith J.E. Repine K.A. Joiner 1988 Pathogenesis of Campylobacter fetus infections. Failure of encapsulated Campylobacter fetus to bind C3b explains serum and phagocytosis resistance J Clin Invest 81 1434–1444.
97. Z. Pei M.J. Blaser 1990 Pathogenesis of Campylobacter fetus infections. Role of surface array proteins in virulence in a mouse model J Clin Invest 85 1036–1043.
98. R. Grogono-Thomas J. Dworkin M.J. Blaser D.G. Newell 2000 Roles of the surface layer proteins of Campylobacter fetus subsp. fetus in ovine abortion Infect Immun 68 1687–1691.
99. M.K. Tummuru M.J. Blaser 1992 Characterization of the Campylobacter fetus sapA promoter: evidence that the sapA promoter is deleted in spontaneous mutant strains J Bacteriol 174 5916–5922.
100. M.J. Blaser E. Wang M.K. Tummuru R. Washburn S. Fujimoto A. Labigne 1994 High-frequency S-layer protein variation in Campylobacter fetus revealed by sapA mutagenesis Mol Microbiol 14 453–462.
101. J. Dworkin M.J. Blaser 1996 Generation of Campylobacter fetus S-layer protein diversity utilizes a single promoter on an invertible DNA segment Mol Microbiol 19 1241–1253.
102. M. Fujita T. Moriya S. Fujimoto N. Hara K. Amako 1997 A deletion in the sapA homologue cluster is responsible for the loss of the S-layer in Campylobacter fetus strain TK Arch Microbiol 167 196–201.
103. L.B. Corbeil G.G. Schurig P.J. Bier A.J. Winter 1975 Bovine veneral vibriosis: antigenic variation of the bacterium during infection Infect Immun 11 240–244.
104. E. Wang M.M. Garcia M.S. Blake Z. Pei M.J. Blaser 1993 Shift in S-layer protein expression responsible for antigenic variation in Campylobacter fetus J Bacteriol 175 4979–4984.
105. M.M. Garcia C.L. Lutze-Wallace A.S. Denes M.D. Eaglesome E. Holst M.J. Blaser 1995 Protein shift and antigenic variation in the S-layer of Campylobacter fetus subsp. venerealis during bovine infection accompanied by genomic rearrangement of sapA homologs J Bacteriol 177 1976–1980.
106. R. Grogono-Thomas M.J. Blaser M. Ahmadi D.G. Newell 2003 Role of S-layer protein antigenic diversity in the immune responses of sheep experimentally challenged with Campylobacter fetus subsp. fetus Infect Immun 71 147–154.
107. J.D. Dubreuil M. Kostrzynska J.W. Austin T.J. Trust 1990 Antigenic differences among Campylobacter fetus S-layer proteins J Bacteriol 172 5035–5043.
108. M.K. Tummuru M.J. Blaser 1993 Rearrangement of sapA homologs with conserved and variable regions in Campylobacter fetus Proc Natl Acad Sci U S A 90 7265–7269.
109. J. Dworkin M.J. Blaser 1997 Nested DNA inversion as a paradigm of programmed gene rearrangement Proc Natl Acad Sci U S A 94 985–990.
110. J. Dworkin O.L. Shedd M.J. Blaser 1997 Nested DNA inversion of Campylobacter fetus S-layer genes is recA dependent J Bacteriol 179 7523–7529.
111. K.C. Ray Z.C. Tu R. Grogono-Thomas D.G. Newell S.A. Thompson M.J. Blaser 2000 Campylobacter fetus sap inversion occurs in the absence of RecA function Infect Immun 68 5663–5667.
112. Z.C. Tu C. Gaudreau M.J. Blaser 2005 Mechanisms underlying Campylobacter fetus pathogenesis in humans: surface-layer protein variation in relapsing infections J Infect Dis 191 2082–2089.