Flagellar motility of the pathogenic spirochetes

Seminars in Cell and Developmental Biology

Volumn 46, Issue , 2015, Pages 104-112

  Wolgemuth, Charles W ^a,b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Bacterial motility; Leptospirosis; Lyme disease; Spirochetes; Syphilis

Indexed keywords

BACTERIAL FLAGELLUM; BACTERIAL OUTER MEMBRANE; BACTERIAL STRUCTURES; BACTERIAL VIRULENCE; BEJEL; BIOPHYSICS; BORRELIA; BORRELIA INFECTION; CELL BODY; CELL MOTILITY; CYTOPLASM; ERYTHEMA CHRONICUM MIGRANS; EXTRACELLULAR MATRIX; FLAGELLAR MOTILITY; HOST PATHOGEN INTERACTION; INNER MEMBRANE; LEPTOSPIRACEAE; LEPTOSPIROSIS; LYME DISEASE; NONHUMAN; PERIODONTAL DISEASE; PINTA; REVIEW; SPIROCHETE; SYPHILIS; TREPONEMA; TREPONEMA CARATEUM; TREPONEMA PALLIDUM; YAWS; ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; FLAGELLUM; HUMAN; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); PERIPLASM; PHYSIOLOGY; SPIROCHETE INFECTION;

ANIMALS; BIOPHYSICAL PHENOMENA; FLAGELLA; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; MOVEMENT; PERIPLASM; SPIROCHAETALES; SPIROCHAETALES INFECTIONS;

EID: 84951277335     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.10.015     Document Type: Review

References (98)

1. WaterCar, 2015. https://www.watercar.com/index.php.
2. Merz A.J., Forest K.T. Bacterial surface motility: slime trails, grapping hooks and nozzles. Curr. Biol. 2002, 12:R297-R303.
3. Harshey R.M. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 2003, 57:249-273.
4. Macnab R.M. Flagella and Motility. Cellular and Molecular Biology 1996, 123-145. ASM Press, Washington, DC. F.C. Neidhardt, R. Curtiss, J.L. Ingraham, E.C.C. Lin, K.B. Low, B. Magasanik, W.S. Reznikoff, M. Riley, M. Schaechter, H.E. Umbarger (Eds.).
5. Rashid M.H., Kornberg A. Inorganic polyphosphate is needed for swimming, swarming and twitching motility of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4885-4890.
6. McCarter L.L. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 2001, 65:445-462.
7. Kearns D.B. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 2010, 8:634-644.
8. Wolfe A.J., Berg H.C. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:6973-6977.
9. Croze O.A., Ferguson G.P., Cates M.E., Poon W.C.K. Migration of chemotactic bacteria in soft agar: role of gel concentration. Biophys. J. 2011, 101:525-534.
10. Botkin D.J., et al. Transposon mutagenesis of infectious Borrelia burgdorferi B31: a pilot study. Molecular Biology of Spirochetes 2006, 13-23. IOS Press, Amsterdam. F.C. Cabello, D. Hulinska, H.P. Godfrey (Eds.).
11. Lin T., Troy E.B., Hu L.T., Gao L., Norris S.J. Transposon mutagenesis as an approach to improved understanding of Borrelia pathogenesis and biology. Front. Cell Infect. Microbiol. 2014, 4:63.
12. Radolf J.D., Hazlett K.R.O., Lukehart S.A. Pathogenesis of Syphilis. Pathogenic Treponema: Molecular and Cellular Biology 2006, Caister Academic Press, Norfolk, UK. J.D. Radolf, S.A. Lukehart (Eds.).
13. Schmid G.P. Epidemiology and clinical similarities of human spirochetal diseases. Rev. Infect. Dis. 1989, 11:S1460-S1469.
14. Sela M.N. Role of Treponema denticola in periodontal diseases. Crit. Rev. Oral Biol. Med. 2001, 12:399-413.
15. Magnuson H.J., et al. Inoculation syphilis in human volunteers. Medicine 1956, 35:33-82.
16. Stokes J.H., Beerman H., Ingraham N.R. Modern Clinical Syphilolology 1944, W.B. Saunders, Philadelphia.
17. Brown W.H., Pearce L. A note on the dissemination of Spirochaeta pallida from the primary focus of infection. Arch. Derm. Syph. 1920, 2:470-472.
18. Benirschke K. Syphilis-the placenta and the fetus. Am. J. Dis. Child 1974, 128:142-143.
19. Harter C., Benirschke K. Fetal syphilis in the first trimester. Am. J. Obstetr. Gynecol. 1976, 124:705-711.
20. Drusin L.M., Rouiller G.C., Chapman G.B. Electron microscopy of Treponema pallidum occurring in a primary lesion. J. Bacteriol. 1969, 97:951-955.
21. Sell S., Salman J., Norris S.J. Reinfection of chancre-immune rabbits with Treponema pallidum, I. Light and immunofluorescence studies. Am. J. Pathol. 1985, 118:248-255.
22. Sell S., Salman J. Demonstration of Treponema pallidum in axons of cutaneous nerves in experimental chancres of rabbits. Sex. Transm. Dis. 1992, 19:1-6.
23. Lukehart S.A. Syphilis. Harrison's Principles of Internal Medicine 2004, McGraw Hill, New York. E. Brauwald, A.S. Faucci, S.L. Hauser, D.L. Longo, J.L. Jameson (Eds.).
24. Antal G.M., Lukehart S.A., Meheus A.Z. The endemic treponematoses. Microbes Infect. 2002, 4:83-94.
25. Mitja O., Asiedu K., Mabey D. Yaws. Lancet 2013, 381:763-773.
26. Dewhirst F.E., et al. The diversity of periodonatal spirochetes by 16S rRNA analysis. Oral Microbiol. Immunol. 2000, 15:196-202.
27. Holt S.C., Ebersole J.L. The oral Spirochetes: their ecology and role in the pathogenesis of periodontal disease. Pathogenic Treponema: Molecular and Cellular Biology 2006, Caister Academic Press, Norfolk. J.D. Radolf, S.A. Lukehart (Eds.).
28. Keyes P.H., Rams T.E. A rational for management of periodontal disease, rapid identification of microbial "therapeutic targets" with phase-contrast microscopy. J. Am. Dent. Assoc. 1983, 106:803-812.
29. Armitage G.C., Dickenson W.R., Jenderseck R.J., Levine S.M., Chanbers D.W. Relationship between the percentage of subgingival spirochetes and the severity of periodontal disease. J. Periodontol. 1982, 53:550-556.
30. Deng Q.D., Han Y., Xia X., Kuramitsu H.K. Effects of the oral spirochete T. denticola on interleukin-8 expression from epithelial cells. Oral Microbiol. Immunol. 2001, 16:185-187.
31. Dandache P., Nadelman R.B. Erythema migrans. Infect. Dis. Clin. North Am. 2008, 22:235-260.
32. Radolf J.D., Caimano M.J., Stevenson B., Hu L.T. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Microbiol. Rev. 2012, 10:87-99.
33. Harman M., et al. The heterogeneous motility of the Lyme disease spirochete in gelatin mimics dissemination through tissue. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3059-3064.
34. Coburn J., Fischer J.R., Leong J.M. Solving a sticky problem: new genetic approaches to host cell adhesion by the Lyme disease spirochete. Mol. Microbiol. 2005, 57:1182-1195.
35. Steere A.C., Coburn J., Glickstein L. The emergence of Lyme disease. J. Clin. Invest. 2004, 113:1093-1101.
36. Salazar J.C., et al. Coevolution of markers of innate and adaptive immunity in skin and peripheral blood of patients with erythema migrans. J. Immunol. 2003, 171:2660-2670.
37. Delneste Y., et al. Interferon-gamma switches monocyte differentiation from dendritic cells to macrophages. Blood 2003, 101:143-150.
38. CMO., et al. Local production of IFN-gamma by invariant NKT cells modulates acute Lyme carditis. J. Immunol. 2009, 182:3728-3734.
39. Menten-Dedoyart C., et al. Neutrophil extracellular traps entrap and kill Borrelia burgdorferi sensu stricto spirochetes and are not affected by Ixodes ricinus tick saliva. J. Immunol. 2012, 189:5393-5401.
40. Vig D.K., Wolgemuth C.W. Spatiotemporal evolution of Erythema migrans, the hallmark rash of Lyme disease. Biophys. J. 2014, 106:763-768.
41. Radolf J.D., Salazar J.C., Dattwyler R.J. Lyme disease in humans. Borrelia: Molecular Biology, Host Interaction and Pathogenesis 2010, Caister Academic Press, Norfolk, UK. J.D. Radolf, D.S. Samuels (Eds.).
42. Sultan S.Z., et al. Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts. Infect. Immun. 2015, 83:1765-1777.
43. Sultan S.Z., et al. Motility is crucial for the infectious life cycle of Borrelia burgdorferi. Infect. Immun. 2013, 81:2012-2021.
44. Sze C.W., Zhang K., Kariu T., Pal U., Li C. Borrelia burgdorferi needs chemotaxis to establish infection in mammals and to accomplish its enzootic cycle. Infect. Immun. 2012, 80:2485-2492.
45. Barbour A.G., Guo B.P. Pathogenesis of relapsing fever. Borrelia: Molecular Biology, Host Interaction and Pathogenesis 2010, Caister Academic Press, Norfolk, UK. D.S. Samuels, J.D. Radolf (Eds.).
46. Evangelista K.V., Coburn J. Leptospira as an emerging pathogen: a review of its biology, pathogenesis and host immune responses. Future Microbiol. 2010, 5:1413-1425.
47. Faine S., Adler B., Bolin C., Perolat P. Leptospira and Leptospirosis 1999, 296-326. MediSci, Melbourne, Australia. 2nd ed.
48. Levett P.N. Leptospirosis. Clin. Microbiol. Rev. 2001, 14:296-326.
49. Liao S., et al. Inactivation of the fliY gene encoding a flagellar motor switch protein attenuates motbility and virulence of Leptospira interrogans strain Lai. BMC Microbiol. 2009, 9:253.
50. Lambert A., et al. FlaA proteins in Leptospira interrogans are essential for motility and virulence but are not required for formation of the flagellum sheath. Infect. Immun. 2012, 80:2019-2025.
51. Paster B.J. Phylum XV. Spirochaetes Garrity and Holt 2001. Bergey's Manual of Systematic Bacteriology 2011, vol. 4:471-566. Springer, New York.
52. Charon N.W., et al. The unique paradigm of spirochete motility and chemotaxis. Annu. Rev. Microbiol. 2012, 66:349-370.
53. Charon N.W., et al. The flat ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 2009, 191:600-607.
54. Berg H.C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 2003, 79:19-54.
55. Carleton O., Charon N.W., Allender P., O'Brien S. Helix Handedness of Leptospira interrogans as determined by scanning electron microscopy. J. Bacteriol. 1979, 137:1413-1416.
56. Goldstein S.F., Charon N.W. Motility of the spirochete Leptospira. Cell Motil. Cytoskel. 1988, 9:101-110.
57. Goldstein S.F., Charon N.W. Multiple-exposure photographic analysis of a motile spirochete. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:4895-4899.
58. Berg H.C., Bromley D.B., Charon N.W. Leptospiral motility. Symp. Soc. Gen. Microbiol. 1978, 285-294.
59. Bromley D.B., Charon N.W. Axial filament involvement in the motility of Leptospira interrogans. J. Bacteriol. 1979, 137(3):1406-1412.
60. Picardeau M., Brenot A., Saint I. First evidence for gene replacement in Leptospira spp. inactivation of L. biflexa flaB results in non-motile mutants deficient in endoflagella. Mol. Microbiol. 2001, 40(1):189-199.
61. Canale-Parola E. The spirochetes. Bergey's Manual of Systematic Biology 1984, Williams and Wilkins, Baltimore, MD. N.R. Krieg, J.G. Holt (Eds.).
62. Socransky S., Listgarten M., Hubersak C., Bial J.J., Morton H.E. Morphological and biochemical differentiation of three types of small oral spirochetes. J. Bacteriol. 1969, 98:878-882.
63. Ruby J.D., et al. Relationship of Treponema denticola periplasmic flagella to irregular cell morphology. J. Bacteriol. 1997, 179(5):1628-1635.
64. Goldstein S.F., Charon N.W., Kreiling J.A. Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:3433-3437.
65. Izard J., et al. Cryo-electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. J. Bacteriol. 2009, 191:7566-7580.
66. Goldstein S.F., Buttle K.F., Charon N.W. Structural analysis of the Leptospiracae and Borrelia burgdorferi by high-voltage electron microscopy. J. Bacteriol. 1996, 178(22):6539-6545.
67. Kudryashev M., et al. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol. Microbiol. 2009, 71:1415-1434.
68. Liu J., et al. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C ring assembly felxion. J. Bacteriol. 2009, 191:5026-5036.
69. Charon N.W., Goldstein S.F. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet. 2002, 36:47-73.
70. Motaleb M.A., et al. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. U.S.A. 2000, 97(20):10899-10904.
71. Sartakova M.L., et al. Complementation of a nonmotile flaB mutant of Borrelia burgdorferi by chromosomal integration of a plasmid containing a wild-type flaB allele. J. Bacteriol. 2001, 183:6558-6564.
72. Kan W., Wolgemuth C.W. The shape and dynamics of the Leptospiraceae. Biophys. J. 2006, 93:54-61.
73. Dombrowski C., et al. The elastic basis for the shape of Borrelia burgdorferi. Biophys. J. 2009, 96:4409-4417.
74. Vig D.K., Wolgemuth C.W. Swimming dynamics of the Lyme disease spirochete. Phys. Rev. Lett. 2012, 109:218104.
75. Wolgemuth C.W., Charon N.W., Goldstein S.F., Goldstein R.E. The flagellar cytoskeleton of the spirochetes. J. Mol. Microbiol. Biotechnol. 2006, 11:221-227.
76. Hovind Hougen K. Ultrastructure of spirochetes isolated from Ixodes ricinus and Ixodes dammini. Yale J. Biol. Med. 1984, 57:543-548.
77. Taylor G.I. Analysis of the swimming of microscopic organisms. Proc. R. Soc. Lond. A 1951, 209:447-461.
78. Taylor G.I. The action of waving cylindrical tails in propelling microorganisms. Proc. R. Soc. Lond. A 1952, 211:225-239.
79. Lauga E., Powers T.R. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 2009, 72:096601.
80. Harman M., Vig D.K., Radolf J.D., Wolgemuth C.W. Viscous dynamics of Lyme disease and syphylis spirochetes reveal flagellar torque and drag. Biophys. J. 2013, 105:2273-2280.
81. Chwang A.T., Winet H., Wu T.Y. A theoretical mechanism of spirochete locomotion. J. Mechanochem. Cell Motility 1974, 3:69-76.
82. Cox D.L., Radolf J.D. Metabolism of the Treponema. Pathogenic Treponema: Molecular and Cellular Biology 2006, Caister Academic Press, Norfolk, UK. J.D. Radolf, S.A. Lukehart (Eds.).
83. Li G., Tang J.X. Low flagellar motor torque and high swimming efficiency of Caulobacter crescentus swarmer cells. Biophys. J. 2006, 91:2726-2734.
84. Berry R.M., Berg H.C. Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14433-14437.
85. Li C., Motaleb M.A., Sal M., Goldstein S.F., Charon N.W. Spirochete periplasmic flagella and motility. J. Mol. Microbiol. Biotechnol. 2000, 2(2):345-354.
86. Charon N.W., Daughtry G.R., McCuskey R.S., Franz G.N. Microcinematographic analysis of tethered Leptospira illini. J. Bacteriol. 1984, 160:1067-1073.
87. Nakamura S., Leshansky A., Magariyama Y., Namba K., Kudo S. Direct measurement of helical cell motion of the spirochete Leptospira. Biophys. J. 2014, 106:47-54.
88. Dunham-Ems S.M., et al. Live imaging reveals a novel, biphasic mode of dissemination of Borrelia burgdorferi within ticks. J. Clin. Invest. 2009, 119:3652-3665.
89. Moriarty T.J., et al. Real-time high resolution 3D imaging of the Lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLOS Pathog. 2008, 4:e1000090.
90. Pal U., et al. OspC facillitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 2004, 113:220-230.
91. Kimsey R.B., Spielman A. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J. Infect. Dis. 1990, 162:1205-1208.
92. Berg H.C. Random Walks in Biology 1983, Princeton University Press, Princeton, NJ.
93. Thakar J., Saadatpour-Moghaddam A., Harvill E.T., Albert R. Constraint-based network model of pathogen-immune system interactions. J. R. Soc. Interface 2009, 6:599-612.
94. Campbell C., Thakar J., Albert R. Network analysis reveals cross-links of the immune pathways activated by bacteria and allergen. Phys. Rev. E 2011, 84:031929.
95. Montgomery R.R., Lusitani D., Chevance AdB, Malawista S.E. Human phagocytic cells in the early innate immune response to Borrelia burgdorferi. J. Infect. Dis. 2002, 185:1773-1779.
96. Keller E.F., Segel L.A. Model for chemotaxis. J. Theor. Biol. 1971, 30:225-234.
97. Banfi E., Cinco M., Perticarari S., Presani G. Rapid flow cytometric studies of Borrelia burgdorferi phagocytosis by human polymorphonuclear leukocytes. J. Appl. Bacteriol. 1989, 67:37-45.
98. Kenedy M.R., Lenhart T.R., Akins D.R. The role of Borrelia burgdorferi outer surface proteins. FEMS Immunol. Med. Microbiol. 2012, 66:1-19.