Comparative molecular analyses of Borrelia burgdorferi sensu stricto strains B31 and N40D10/E9 and determination of their pathogenicity

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Chan, Kamfai ^a   Awan, Mehwish ^a   Barthold, Stephen W ^b   Parveen, Nikhat ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adherence; B31; Borrelia burgdorferi strains; Lyme disease; N40; Pathogenesis; Tissue colonization

Indexed keywords

ADHESIN; FIBRONECTIN; GLYCOSAMINOGLYCAN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL STRAIN; BORRELIA BURGDORFERI; COMPARATIVE STUDY; IN VITRO STUDY; INOCULATION; LYME DISEASE; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PHYLOGENY; PREDICTION; SPIROCHETE; VERO CELL;

ANIMALS; BACTERIAL ADHESION; BORRELIA BURGDORFERI; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; EUROPE; FEMALE; HUMANS; LYME DISEASE; MICE; MICE, INBRED C3H; UNITED STATES; VERO CELLS; VIRULENCE; VIRULENCE FACTORS;

BORRELIA BURGDORFERI; MUS; SPIROCHAETALES;

EID: 84864330149     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-157     Document Type: Article

References (117)

1. The early clinical manifestations of Lyme disease. Steere AC, Bartenhagen NH, Craft JE, Ann Intern Med 1983 99 76 82 6859726 (Pubitemid 13066663)
2. Lyme disease-a tick-borne spirochetosis. Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP, Science 1982 216 4552 1317 1319 10.1126/science.7043737 7043737
3. Lyme disease. Steere AC, N Engl J Med 2001 345 2 115 125 10.1056/NEJM200107123450207 11450660 (Pubitemid 32640193)
4. Lyme borreliosis. Nadelman RB, Wormser GP, Lancet 1998 352 9127 557 565 10.1016/S0140-6736(98)01146-5 9716075 (Pubitemid 28372237)
5. Clinical Clostridium difficile: clonality and pathogenicity locus diversity. Dingle KE, Griffiths D, Didelot X, Evans J, Vaughan A, Kachrimanidou M, Stoesser N, Jolley KA, Golubchik T, Harding RM, et al. PLoS One 2011 6 5 19993 10.1371/journal.pone.0019993 21625511
6. A variable region within the genome of Streptococcus pneumoniae contributes to strain-strain variation in virulence. Harvey RM, Stroeher UH, Ogunniyi AD, Smith-Vaughan HC, Leach AJ, Paton JC, PLoS One 2011 6 5 19650 10.1371/journal.pone.0019650 21573186
7. Polymorphisms in the intermediate region of VacA impact Helicobacter pylori-induced disease development. Jones KR, Jang S, Chang JY, Kim J, Chung IS, Olsen CH, Merrell DS, Cha JH, J Clin Microbiol 2011 49 1 101 110 10.1128/JCM.01782-10 21084502
8. Comparative analysis of virulence genes, genetic diversity, and phylogeny of Shiga toxin 2 g and heat-stable enterotoxin STIa encoding Escherichia coli isolates from humans, animals, and environmental sources. Prager R, Fruth A, Busch U, Tietze E, International journal of medical microbiology: IJMM 2011 301 3 181 191 10.1016/j.ijmm.2010.06.003 20728406
9. Comparative genome analysis of a large Dutch Legionella pneumophila strain collection identifies five markers highly correlated with clinical strains. Yzerman E, den Boer J, Caspers M, Almal A, Worzel B, van der Meer W, Montijn R, Schuren F, BMC Genomics 2010 11 433 10.1186/1471-2164-11-433 20630115
10. Comparative genome analyses of the pathogenic Yersiniae based on the genome sequence of Yersinia enterocolitica strain 8081. Thomson NR, Howard S, Wren BW, Prentice MB, Adv Exp Med Biol 2007 603 2 16 10.1007/978-0-387-72124-8-1 17966400
11. Treponema pallidum strain-specific differences in neuroinvasion and clinical phenotype in a rabbit model. Tantalo LC, Lukehart SA, Marra CM, J Infect Dis 2005 191 1 75 80 10.1086/426510 15593006 (Pubitemid 40041403)
12. Pathogenicity islands: a molecular toolbox for bacterial virulence. Gal-Mor O, Finlay BB, Cell Microbiol 2006 8 11 1707 1719 10.1111/j.1462-5822. 2006.00794.x 16939533 (Pubitemid 44530664)
13. Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Grimm D, Tilly K, Byram R, Stewart PE, Krum JG, Bueschel DM, Schwan TG, Policastro PF, Elias AF, Rosa PA, Proc Natl Acad Sci U S A 2004 101 9 3142 3147 10.1073/pnas.0306845101 14970347 (Pubitemid 38327748)
14. OspC facilitates Borrelia burgdorferiinvasion of Ixodes scapularis salivary glands. Pal U, Yang X, Chen M, Bockenstedt LK, Anderson JF, Flavell RA, Norgard MV, Fikrig E, J Clin Invest 2004 113 2 220 230 14722614 (Pubitemid 38544207)
15. Infection with multiple strains of Borrelia burgdorferi sensu stricto in patients with Lyme disease. Seinost G, Golde WT, Berger BW, Dunn JJ, Qiu D, Dunkin DS, Dykhuizen DE, Luft BJ, Dattwyler RJ, Arch Dermatol 1999 135 11 1329 1333 10.1001/archderm.135.11.1329 10566830
16. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Wang IN, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, Luft BJ, Genet 1999 151 1 15 30 (Pubitemid 29031873)
17. OspC diversity in Borrelia burgdorferi: different hosts are different niches. Brisson D, Dykhuizen DE, Genetics 2004 168 2 713 722 10.1534/genetics.104.028738 15514047 (Pubitemid 39491451)
18. Demonstration of OspC type diversity in invasive human lyme disease isolates and identification of previously uncharacterized epitopes that define the specificity of the OspC murine antibody response. Earnhart CG, Buckles EL, Dumler JS, Marconi RT, Infect Immun 2005 73 12 7869 7877 10.1128/IAI.73.12.7869- 7877.2005 16299277 (Pubitemid 41740270)
19. Borrelia burgdorferi sensu stricto invasiveness is correlated with OspC-plasminogen affinity. Lagal V, Portnoi D, Faure G, Postic D, Baranton G, Microbes Infect 2006 8 3 645 652 10.1016/j.micinf.2005.08.017 16513394
20. Molecular typing of Borrelia burgdorferi from Lyme disease patients by PCR-restriction fragment length polymorphism analysis. Liveris D, Wormser GP, Nowakowski J, Nadelman R, Bittker S, Cooper D, Varde S, Moy FH, Forseter G, Pavia CS, et al. J Clinic Microbiol 1996 34 5 1306 1309 (Pubitemid 26126916)
21. Genetic diversity of Borrelia burgdorferi in lyme disease patients as determined by culture versus direct PCR with clinical specimens. Liveris D, Varde S, Iyer R, Koenig S, Bittker S, Cooper D, McKenna D, Nowakowski J, Nadelman RB, Wormser GP, et al. J Clin Microbiol 1999 37 3 565 569 9986813 (Pubitemid 29091265)
22. Quantitative detection of Borrelia burgdorferi in 2-millimeter skin samples of erythema migrans lesions: correlation of results with clinical and laboratory findings. Liveris D, Wang G, Girao G, Byrne DW, Nowakowski J, McKenna D, Nadelman R, Wormser GP, Schwartz I, J Clin Microbiol 2002 40 4 1249 1253 10.1128/JCM.40.4.1249-1253.2002 11923340 (Pubitemid 34279884)
23. Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. Wormser GP, Liveris D, Nowakowski J, Nadelman RB, Cavaliere LF, McKenna D, Holmgren D, Schwartz I, J Infect Dis 1999 180 3 720 725 10.1086/314922 10438360 (Pubitemid 29411358)
24. Borrelia burgdorferi genetic markers and disseminated disease in patients with early Lyme disease. Jones KL, Glickstein LJ, Damle N, Sikand VK, McHugh G, Steere AC, J Clin Microbiol 2006 44 12 4407 4413 10.1128/JCM.01077-06 17035489 (Pubitemid 44937072)
25. Borrelia burgdorferi gene expression in vivo and spirochete pathogenicity. Anguita J, Samanta S, Revilla B, Suk K, Das S, Barthold SW, Fikrig E, Infect Immun 2000 68 3 1222 1230 10.1128/IAI.68.3.1222-1230.2000 10678930 (Pubitemid 30108514)
26. Inoculation of nonhuman primates with the N40 strain of Borrelia burgdorferi leads to a model of Lyme neuroborreliosis faithful to the human disease. Pachner AR, Delaney E, O'Neill T, Major E, Neurology 1995 45 1 165 172 10.1212/WNL.45.1.165 7824109
27. Borrelia burgdorferi lacking DbpBA exhibit an early survival defect during experimental infection. Weening EH, Parveen N, Trzeciakowski JP, Leong JM, Hook M, Skare JT, Infect Immun 2008 76 12 5694 5705 10.1128/IAI.00690-08 18809667
28. Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. Barthold SW, Moody KD, Terwilliger GA, Duray PH, Jacoby RO, Steere AC, J Infect Dis 1988 157 4 842 846 10.1093/infdis/157.4.842 3258003 (Pubitemid 18093753)
29. Detection of established virulence genes and plasmids to differentiate Borrelia burgdorferi strains. Chan K, Casjens S, Parveen N, Infect Immun 2012 80 4) 1519 1529 22290150
30. Whole-genome sequences of thirteen isolates of Borrelia burgdorferi. Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu WG, Dunn JJ, Mongodin EF, Luft BJ, J Bacteriol 2011 193 4 1018 1020 10.1128/JB.01158-10 20935092
31. Genetic heterogeneity of Borrelia burgdorferi in the United States. Mathiesen DA, Oliver JH Jr, Kolbert CP, Tullson ED, Johnson BJ, Campbell GL, Mitchell PD, Reed KD, Telford SR, Anderson JF 3rd, et al. The Journal of infectious diseases 1997 175 1) 98 107 8985202 (Pubitemid 27020830)
32. Disease severity in a murine model of lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. Wang G, Ojaimi C, Wu H, Saksenberg V, Iyer R, Liveris D, McClain SA, Wormser GP, Schwartz I, J Infect Dis 2002 186 6 782 791 10.1086/343043 12198612 (Pubitemid 35013430)
33. Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Wang G, Ojaimi C, Iyer R, Saksenberg V, McClain SA, Wormser GP, Schwartz I, Infect Immun 2001 69 7 4303 4312 10.1128/IAI.69.7.4303-4312.2001 11401967 (Pubitemid 32574426)
34. Borrelia burgdorferi RST1 (OspC type A) genotype is associated with greater inflammation and more severe Lyme disease. Strle K, Jones KL, Drouin EE, Li X, Steere AC, Ame J Pathol 2011 178 6 2726 2739 10.1016/j.ajpath.2011.02.018
35. Lyme disease susceptible and resistant strains of laboratory mice infected with Borrelia burgdorferi. Armstrong AL, Barthold SW, Persing DH, Beck DS, Amer J Trop Med Hyg 1992 47 249 258
36. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Barthold SW, Persing DH, Armstrong AL, Peeples RA, Am J Pathol 1991 139 2 263 273 1867318
37. Infection and inflammation in skeletal muscle from nonhuman primates infected with different genospecies of the Lyme disease spirochete Borrelia burgdorferi. Cadavid D, Bai Y, Dail D, Hurd M, Narayan K, Hodzic E, Barthold SW, Pachner AR, Infect Immun 2003 71 12 7087 7098 10.1128/IAI.71.12.7087-7098.2003 14638799 (Pubitemid 37475341)
38. Adaptation of the Lyme disease spirochaete to the mammalian host environment results in enhanced glycosaminoglycan and host cell binding. Parveen N, Caimano M, Radolf JD, Leong JM, Mol Microbiol 2003 47 5 1433 1444 10.1046/j.1365-2958.2003.03388.x 12603746 (Pubitemid 36307862)
39. A portuguese isolate of Borrelia lusitaniae induces disease in C3H/HeN mice. Zeidner NS, Nuncio MS, Schneider BS, Gern L, Piesman J, Brandao O, Filipe AR, J Med Microbiol 2001 50 12 1055 1060 11761189 (Pubitemid 33108911)
40. Antibody-mediated disease remission in the mouse model of lyme borreliosis. Barthold SW, Hodzic E, Tunev S, Feng S, Infect Immun 2006 74 8 4817 4825 10.1128/IAI.00469-06 16861670 (Pubitemid 44157269)
41. Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Probert WS, Johnson BJ, Mol Microbiol 1998 30 5 1003 1015 10.1046/j.1365-2958.1998.01127.x 9988477 (Pubitemid 28550124)
42. Variable small protein (Vsp)-dependent and Vsp-independent pathways for glycosaminoglycan recognition by relapsing fever spirochaetes. Magoun L, Zuckert WR, Robbins D, Parveen N, Alugupalli KR, Schwan TG, Barbour AG, Leong JM, Mol Microbiol 2000 36 4 886 897 10.1046/j.1365-2958.2000.01906.x 10844676 (Pubitemid 30326534)
43. Decorin-binding proteins A and B confer distinct mammalian cell type-specific attachment by Borrelia burgdorferi, the Lyme disease spirochete. Fischer JR, Parveen N, Magoun L, Leong JM, Proc Natl Acad Sci USA 2003 100 12 7307 7312 10.1073/pnas.1231043100 12773620 (Pubitemid 36706434)
44. Borrelia burgdorferi BmpA is a laminin-binding protein. Verma A, Brissette CA, Bowman A, Stevenson B, Infect Immun 2009 77 11 4940 4946 10.1128/IAI.01420-08 19703983
45. Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Seshu J, Esteve-Gassent MD, Labandeira-Rey M, Kim JH, Trzeciakowski JP, Hook M, Skare JT, Mol Microbiol 2006 59 5 1591 1601 10.1111/j.1365-2958.2005.05042.x 16468997
46. Molecular mechanisms involved in vascular interactions of the Lyme disease pathogen in a living host. Norman MU, Moriarty TJ, Dresser AR, Millen B, Kubes P, Chaconas G, PLoS Pathog 2008 4 10 1000169 10.1371/journal.ppat.1000169 18833295
47. Proteoglycans: Structures and interactions. Kjellen L, Lindahl U, Annu Rev Biochem 1991 60 443 475 10.1146/annurev.bi.60.070191.002303 1883201
48. Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. Wadstrom T, Ljungh A, J Med Microbiol 1999 48 3 223 233 10.1099/00222615-48-3-223 10334589 (Pubitemid 29371567)
49. Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi. Leong JM, Morrissey PE, Ortega-Barria E, Pereira MEA, Coburn J, Infect Immun 1995 63 874 883 7532628
50. Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Parveen N, Leong JM, Mol Microbiol 2000 35 5 1220 1234 10.1046/j.1365-2958.2000.01792.x 10712702 (Pubitemid 30137790)
51. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Guo BP, Norris SJ, Rosenberg LC, Hook M, Infect Immun 1995 63 9 3467 3472 7642279
52. Decorin-binding adhesins from Borrelia burgdorferi. Guo BP, Brown EL, Dorward DW, Rosenberg LC, Hook M, Mol Microbiol 1998 30 4 711 723 10.1046/j.1365-2958.1998.01103.x 10094620 (Pubitemid 28528591)
53. Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans. Fischer JR, LeBlanc KT, Leong JM, Infect Immun 2006 74 1 435 441 10.1128/IAI.74.1.435-441.2006 16368999 (Pubitemid 43023100)
54. Characterization of a candidate Borrelia burgdorferi b3-integrin ligand identified using a phage display library. Coburn J, Chege W, Magoun L, Bodary S, Leong JM, Mol Microbiol 1999 34 926 940 10.1046/j.1365-2958.1999.01654.x 10594819 (Pubitemid 30000311)
55. Targeted mutation of the outer membrane protein P66 disrupts attachment of the Lyme disease agent, Borrelia burgdorferi, to integrin alphavbeta3. Coburn J, Cugini C, Proc Natl Acad Sci U S A 2003 100 12 7301 7306 10.1073/pnas.1131117100 12748384 (Pubitemid 36706433)
56. Molecular analysis of a 66-kDa protein associated with the outer membrane of Lyme disease Borrelia. Bunikis J, Noppa L, Bergstrom S, FEMS Microbiol Lett 1995 131 2 139 145 10.1111/j.1574-6968.1995.tb07768.x 7557322
57. The Oms66 (p66) protein is a Borrelia burgdorferi porin. Skare JT, Mirzabekov TA, Shang ES, Blanco DR, Erdjument-Bromage H, Bunikis J, Bergstrom S, Tempst P, Kagan BL, Miller JN, et al. Infect Immun 1997 65 9 3654 3661 9284133 (Pubitemid 27398121)
58. Adherence and entry of Borrelia burgdorferi in Vero cells. Hechemy KE, Samsonoff WA, Harris HL, McKee M, J Med Microb 1992 36 229 238 10.1099/00222615-36-4-229
59. Structural requirements for glycosaminoglycan recognition by the Lyme disease spirochete, Borrelia burgdorferi. Leong JM, Robbins D, Rosenfeld L, Lahiri B, Parveen N, Infect Immun 1998 66 6045 6048 9826395 (Pubitemid 28531875)
60. Interaction of Lyme disease spirochetes with cultured eucaryotic cells. Thomas DD, Comstock LE, Infect Imm 1989 57 1324 1326 (Pubitemid 19087887)
61. Strain variation in glycosaminoglycan recognition influences cell-type-specific binding by Lyme disease spirochetes. Parveen N, Robbins D, Leong JM, Infect Immun 1999 67 4 1743 1749 10085013 (Pubitemid 29144392)
62. Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells. Leong JM, Wang H, Magoun L, Field JA, Morrissey PE, Robbins D, Tatro JB, Coburn J, Parveen N, Infect Immun 1998 66 3 994 999 9488387 (Pubitemid 28101138)
63. Interaction between Borrelia burgdorferi and endothelium in vitro. Szczepanski A, Furie MB, Benach JL, Lane BP, Fleit HB, J Clin Invest 1990 85 1637 1647 10.1172/JCI114615 2332509 (Pubitemid 20176462)
64. Adherence of the Lyme disease spirochete to glial cells and cells of glial origin. Garcia-Monco JC, Fernandez-Villar B, Benach JL, J Infect Dis 1989 160 497 506 10.1093/infdis/160.3.497 2760500
65. Biological characteristics and viral susceptibility of an African green monkey kidney cell line (Vero). Rhim JS, Schell K, Creasy B, Case W, Proc Soc Exp Biol Med 1969 132 2 670 678 4982209
66. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Edgell CJ, McDonald CC, Graham JB, Proc Natl Acad Sci USA 1983 80 12 3734 3737 10.1073/pnas.80.12.3734 6407019 (Pubitemid 13063134)
67. Endothelium specific Weibel-Palade bodies in a continuous human cell line, EA.hy926. Edgell CJ, Haizlip JE, Bagnell CR, Packenham JP, Harrison P, Wilbourn B, Madden VJ, In Vitro Cell Dev Biol 1990 26 12 1167 1172 10.1007/BF02623694 2079463
68. Differentiated rat glial cell strain in tissue culture. Benda P, Lightbody J, Sato G, Levine L, Sweet W, Science 1968 161 3839 370 371 10.1126/science.161.3839.370 4873531
69. Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, Glowacki J, Arbiser JL, Apperley JF, J Clin Invest 1994 94 6 2307 2316 10.1172/JCI117595 7989586
70. Proteoglycan production by immortalized human chondrocyte cell lines cultured under conditions that promote expression of the differentiated phenotype. Kokenyesi R, Tan L, Robbins JR, Goldring MB, Arch Biochem Biophys 2000 383 1 79 90 10.1006/abbi.2000.2044 11097179
71. Molecular phenotyping of human chondrocyte cell lines T/C-28a2, T/C-28a4, and C-28/I2. Finger F, Schorle C, Zien A, Gebhard P, Goldring MB, Aigner T, Arthritis Rheum 2003 48 12 3395 3403 10.1002/art.11341 14673991 (Pubitemid 37531906)
72. Distinct characteristics of resistance to Borrelia burgdorferi-induced arthritis in C57BL/6 N mice. Ma Y, Seiler KP, Eichwald EJ, Weis JH, Teuscher C, Weis JJ, Infect Immun 1998 66 1 161 168 9423853
73. Lyme borreliosis in selected strains and ages of laboratory mice. Barthold SW, Beck DS, Hansen GM, Terwilliger GA, Moody KD, J Infect Dis 1990 162 1 133 138 10.1093/infdis/162.1.133 2141344 (Pubitemid 20223961)
74. Localized production of IL-10 suppresses early inflammatory cell infiltration and subsequent development of IFN-gamma-mediated Lyme arthritis. Sonderegger FL, Ma Y, Maylor-Hagan H, Brewster J, Huang X, Spangrude GJ, Zachary JF, Weis JH, Weis JJ, J Immunol 2012 188 3 1381 1393 10.4049/jimmunol.1102359 22180617
75. Short report: Association of macrophage inflammatory response and cell death after in vitro Borrelia burgdorferi infection with arthritis resistance. Glickstein LJ, Coburn JL, Am J Trop Med Hyg 2006 75 5 964 967 17123997 (Pubitemid 351627550)
76. Outer surface protein C is a dissemination-facilitating factor of Borrelia burgdorferi during mammalian infection. Seemanapalli SV, Xu Q, McShan K, Liang FT, PLoS One 2010 5 12 15830 10.1371/journal.pone.0015830 21209822
77. Two regulatory elements required for enhancing ospA expression in Borrelia burgdorferi grown in vitro but repressing its expression during mammalian infection. Xu Q, McShan K, Liang FT, Microbiology 2010 156 Pt 7 2194 2204 20395273
78. Both decorin-binding proteins A and B are critical for overall virulence of Borrelia burgdorferi. Shi Y, Xu Q, McShan K, Liang FT, Infect Immun 2008 76 3 1239 1246 10.1128/IAI.00897-07 18195034 (Pubitemid 351428087)
79. Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Sze CW, Li C, Infect Immun 2011 79 3 1270 1279 10.1128/IAI.00871-10 21173314
80. The Borrelia burgdorferi outer-surface protein ErpX binds mammalian laminin. Brissette CA, Verma A, Bowman A, Cooley AE, Stevenson B, Microbiology 2009 155 Pt 3 863 872 19246757
81. Borrelia burgdorferi bind to epithelial cell proteoglycan. Isaacs R, J Clin Investig 1994 93 809 819 10.1172/JCI117035 8113413 (Pubitemid 24072824)
82. CsrA modulates levels of lipoproteins and key regulators of gene expression critical for pathogenic mechanisms of Borrelia burgdorferi. Karna SL, Sanjuan E, Esteve-Gassent MD, Miller CL, Maruskova M, Seshu J, Infection and immunity 2011 79 2 732 744 10.1128/IAI.00882-10 21078860
83. Gene regulation in Borrelia burgdorferi. Samuels DS, Annu Rev Microbiol 2011 65 479 499 10.1146/annurev.micro.112408.134040 21801026
84. The OspE-related proteins inhibit complement deposition and enhance serum resistance of Borrelia burgdorferi, the lyme disease spirochete. Kenedy MR, Akins DR, Infect Immun 2011 79 4 1451 1457 10.1128/IAI.01274-10 21282413
85. Characterization of a conditional bosR mutant in Borrelia burgdorferi. Hyde JA, Shaw DK, Smith R 3rd, Trzeciakowski JP, Skare JT, Infect Immun 2010 78 1 265 274 10.1128/IAI.01018-09 19858309
86. Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. Pal U, Wang P, Bao F, Yang X, Samanta S, Schoen R, Wormser GP, Schwartz I, Fikrig E, J Exp Med 2008 205 1 133 141 10.1084/jem.20070962 18166585 (Pubitemid 351185721)
87. Borrelia burgdorferi lipoprotein BmpA activates pro-inflammatory responses in human synovial cells through a protein moiety. Yang X, Izadi H, Coleman AS, Wang P, Ma Y, Fikrig E, Anguita J, Pal U, Microbes and infection / Institut Pasteur 2008 10 12-13 1300 1308 18725314
88. Characterization of unique regions of Borrelia burgdorferi surface-located membrane protein 1. Yang X, Lenhart TR, Kariu T, Anguita J, Akins DR, Pal U, Infect Immun 2010 78 11 4477 4487 10.1128/IAI.00501-10 20696833
89. A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi. Ouyang Z, He M, Oman T, Yang XF, Norgard MV, Proceedings of the National Academy of Sciences of the United States of America 2009 106 9 3449 3454 10.1073/pnas.0812999106 19218460
90. Transcription and genetic analyses of a putative N-acetylmuramyl-L- alanine amidase in Borrelia burgdorferi. Yang Y, Li C, FEMS Microbiol Lett 2009 290 2 164 173 19025570
91. sodA is essential for virulence of Borrelia burgdorferi in the murine model of Lyme disease. Esteve-Gassent MD, Elliott NL, Seshu J, Mol Microbiol 2009 71 3 594 612 10.1111/j.1365-2958.2008.06549.x 19040638
92. The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Jewett MW, Lawrence K, Bestor AC, Tilly K, Grimm D, Shaw P, VanRaden M, Gherardini F, Rosa PA, Mol Microbiol 2007 64 5 1358 1374 10.1111/j.1365-2958.2007.05746.x 17542926 (Pubitemid 46849024)
93. Regulation of the virulence determinant OspC by bbd18 on linear plasmid lp17 of Borrelia burgdorferi. Sarkar A, Hayes BM, Dulebohn DP, Rosa PA, J Bacteriol 2011 193 19 5365 5373 10.1128/JB.01496-10 21784941
94. CspA-mediated binding of human factor H inhibits complement deposition and confers serum resistance in Borrelia burgdorferi. Kenedy MR, Vuppala SR, Siegel C, Kraiczy P, Akins DR, Infection and immunity 2009 77 7 2773 2782 10.1128/IAI.00318-09 19451251
95. Carbon storage regulator A (CsrA(Bb)) is a repressor of Borrelia burgdorferi flagellin protein FlaB. Sze CW, Morado DR, Liu J, Charon NW, Xu H, Li C, Molecular microbiology 2011 82 4 851 864 10.1111/j.1365-2958.2011.07853.x 21999436
96. Oligopeptide permease A5 modulates vertebrate host-specific adaptation of Borrelia burgdorferi. Raju BV, Esteve-Gassent MD, Karna SL, Miller CL, Van Laar TA, Seshu J, Infection and immunity 2011 79 8 3407 3420 10.1128/IAI.05234-11 21628523
97. Identification and function of the RNA chaperone Hfq in the Lyme disease spirochete Borrelia burgdorferi. Lybecker MC, Abel CA, Feig AL, Samuels DS, Molecular microbiology 2010 78 3 622 635 10.1111/j.1365-2958.2010.07374.x 20815822
98. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Seinost G, Dykhuizen DE, Dattwyler RJ, Golde WT, Dunn JJ, Wang IN, Wormser GP, Schriefer ME, Luft BJ, Infect Immun 1999 67 7 3518 3524 10377134 (Pubitemid 29291524)
99. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Wang G, van Dam AP, Schwartz I, Dankert J, Clin Microbiol Rev 1999 12 4 633 653 10515907 (Pubitemid 29484751)
100. Evidence for lateral transfer and recombination in OspC variation in Lyme disease Borrelia. Livey I, Gibbs CP, Schuster R, Dorner F, Mol Microbiol 1995 18 2 257 269 10.1111/j.1365-2958.1995.mmi-18020257.x 8709845
101. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, et al. Nature 1997 390 6660 580 586 10.1038/37551 9403685 (Pubitemid 28016185)
102. Bioluminescent imaging of Borrelia burgdorferi in vivo demonstrates that the fibronectin-binding protein BBK32 is required for optimal infectivity. Hyde JA, Weening EH, Chang M, Trzeciakowski JP, Hook M, Cirillo JD, Skare JT, Molecular microbiology 2011 82 1 99 113 10.1111/j.1365-2958.2011.07801.x 21854463
103. Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Li X, Liu X, Beck DS, Kantor FS, Fikrig E, Infect Immun 2006 74 6 3305 3313 10.1128/IAI.02035-05 16714558 (Pubitemid 43794518)
104. An analysis of spirochete load, strain, and pathology in a model of tick-transmitted Lyme borreliosis. Zeidner NS, Schneider BS, Dolan MC, Piesman J, Vector Borne Zoonotic Dis 2001 1 1 35 44 10.1089/153036601750137642 12653134
105. Long-term study of cell-mediated responses to Borrelia burgdorferi in the laboratory mouse. de Souza M, Smith A, Beck D, Terwilliger G, Fikrig E, Barthold S, Infect Immun 1993 61 1814 1822 8478071 (Pubitemid 23145880)
106. Evidence for B-lymphocyte mitogen activity in Borrelia burgdorferi-infected mice. Yang L, Ma Y, Schoenfield R, Griffiths M, Eichwald E, Araneo B, Weis JJ, Infect Immun 1992 60 3033 3041 1639470
107. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Fraser CM, Norris SJ, Weinstock GM, White O, Sutton GG, Dodson R, Gwinn M, Hickey EK, Clayton R, Ketchum KA, et al. Science 1998 281 5375 375 388 9665876 (Pubitemid 28340777)
108. Genetic variation analysis of Vibrio cholerae using multilocus sequencing typing and multi-virulence locus sequencing typing. Teh CS, Chua KH, Thong KL, Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 2011 11 5 1121 1128 21511055
109. The role of outer surface protein D in the Borrelia burgdorferi life cycle. Li X, Neelakanta G, Liu X, Beck DS, Kantor FS, Fish D, Anderson JF, Fikrig E, Infect Immun 2007 75 9 4237 4244 10.1128/IAI.00632-07 17620358 (Pubitemid 47378079)
110. A tightly regulated surface protein of Borrelia burgdorferi is not essential to the mouse-tick infectious cycle. Stewart PE, Bestor A, Cullen JN, Rosa PA, Infect Immun 2008 76 5 1970 1978 10.1128/IAI.00714-07 18332210 (Pubitemid 351656129)
111. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Tilly K, Krum JG, Bestor A, Jewett MW, Grimm D, Bueschel D, Byram R, Dorward D, Vanraden MJ, Stewart P, et al. Infect Immun 2006 74 6 3554 3564 10.1128/IAI.01950-05 16714588 (Pubitemid 43794547)
112. Isolation and cultivation of Lyme disease spirochetes. Barbour AG, Yale J Biol Med 1984 57 521 525 6393604 (Pubitemid 15151039)
113. Cultured mammalian cells attach to the invasin protein of Yersinia pseudotuberculosis. Isberg RR, Leong JM, Proc Natl Acad Sci U S A 1988 85 18 6682 6686 10.1073/pnas.85.18.6682 3413117
114. High resolution two-dimensional electrophoresis of proteins. O'Farrell PH, J Biol Chem 1975 250 4007 4021 236308
115. Computerized quantitative analysis of coomassie-blue-stained serum proteins separated by two-dimensional electrophoresis. Burgess-Cassler A, Johansen JJ, Santek DA, Ide JR, Kendrick NC, Clin Chem 1989 35 12 2297 2304 2480196 (Pubitemid 20017684)
116. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Oakley BR, Kirsch DR, Morris NR, Anal Biochem 1980 105 2 361 363 6161559
117. Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency. Barthold SW, Sidman CL, Smith AL, Am J Trop Med Hyg 1992 47 5 605 613 1449201