The heterogeneous motility of the Lyme disease spirochete in gelatin mimics dissemination through tissue

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 8, 2012, Pages 3059-3064

  Harman, Michael W ^a   Dunham Ems, Star M ^a   Caimano, Melissa J ^a   Belperron, Alexia A ^b   Bockenstedt, Linda K ^b   Fu, Henry C ^c   Radolf, Justin D ^a   Wolgemuth, Charles W ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Nevada   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATIN; METHYLCELLULOSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; BORRELIA BURGDORFERI; DERMIS; EXTRACELLULAR MATRIX; FLOW KINETICS; HOST PATHOGEN INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPIROCHETE;

ANIMALS; BACTERIAL ADHESION; BORRELIA BURGDORFERI; DERMIS; GELATIN; KINETICS; LYME DISEASE; METHYLCELLULOSE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MOVEMENT; RHEOLOGY; SOLUTIONS; TIME-LAPSE IMAGING;

EID: 84857402406     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114362109     Document Type: Article

References (40)

1. Wolgemuth CW (2011) Biomechanics of cell motility. Comprehensive Biomechanics, ed Wirtz D (Elsevier, Amsterdam), Vol 7, in press.
2. Taylor GI (1951) Analysis of the swimming of microscopic organisms. Proc R Soc Lond A Math Phys Sci 209:447-461.
3. Taylor GI (1952) The action of waving cylindrical tails in propelling microorganisms. Proc R Soc Lond A Math Phys Sci 211:225-239.
4. Purcell EM (1977) Life at low Reynolds number. Am J Phys 45:3-11.
5. Croll NA (1970) The Behavior of Nematodes: Their Activity, Senses and Responses (Edward Arnold, London).
6. Fang-Yen C, et al. (2010) Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 107:20323-20328.
7. Shen XN, Arratia PE (2011) Undulatory swimming in viscoelastic fluids. Phys Rev Lett 106:208101.
8. Suarez SS, Dai XB (1992) Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. Biol Reprod 46:686-691.
9. Fu HC, Powers TR, Wolgemuth CW (2007) Theory of swimming filaments in viscoelastic media. Phys Rev Lett 99:258101.
10. Fu HC, Wolgemuth CW, Powers TR (2008) Beating patterns of filaments in viscoelastic fluids. Phys Rev E Stat Nonlin Soft Matter Phys 78:041913.
11. Fu H, Wolgemuth CW, Powers TR (2009) Swimming speeds of filaments in nonlinearly viscoelastic fluids. Phys Fluids 21:033102.
12. Fu HC, Shenoy VB, Powers TR (2011) Low Reynolds-number swimming in gels. Eur Phys Lett 91:24002.
13. Lauga E (2007) Propulsion in a viscoelastic fluid. Phys Fluids 19:083104.
14. Fulford GR, Katz DF, Powell RL (1998) Swimming of spermatozoa in a linear viscoelastic fluid. Biorheology 35:295-309. (Pubitemid 29215049)
15. Goldstein SF, et al. (2010) The chic motility and chemotaxis of Borrelia burgdorferi. Borrelia: Molecular Biology, Host Interaction and Pathogenesis, eds Samuels DS, Radolf JD (Caister Academic, Norfolk, UK), pp 167-188.
16. Charon NW, Goldstein SF (2002) Genetics of motility and chemotaxis of a fascinating group of bacteria: The spirochetes. Annu Rev Genet 36:47-73. (Pubitemid 36109183)
17. Wolgemuth CW, Charon NW, Goldstein SF, Goldstein RE (2006) The flagellar cyto-skeleton of the spirochetes. J Mol Microbiol Biotechnol 11:221-227.
18. Dombrowski C, et al. (2009) The elastic basis for the shape of Borrelia burgdorferi. Biophys J 96:4409-4417.
19. Goldstein SF, Charon NW, Kreiling JA (1994) Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc Natl Acad Sci USA 91:3433-3437. (Pubitemid 24130251)
20. Haake DA (2010) Introduction. Borrelia: Molecular Biology, Host Interaction and Pathogenesis, eds Samuels DS, Radolf JD (Caister Academic, Norfolk, UK), pp 1-6.
21. Dunham-Ems SM, et al. (2009) Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 119:3652-3665.
22. Pal U, Fikrig E (2010) Tick interactions. Borrelia: Molecular Biology, Host Interaction and Pathogenesis, eds Samuels DS, Radolf JD (Caister Academic, Norfolk, UK), pp 279-298.
23. Moriarty TJ, et al. (2008) Real-time high resolution 3D imaging of the lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLoS Pathog 4:e1000090.
24. Cabello FC, Godfrey HP, Newman SA (2007) Hidden in plain sight: Borrelia burgdorferi and the extracellular matrix. Trends Microbiol 15:350-354. (Pubitemid 47126852)
25. Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26: 146-155. (Pubitemid 46401227)
26. Zambrano MC, Beklemisheva AA, Bryksin AV, Newman SA, Cabello FC (2004) Borrelia burgdorferi binds to, invades, and colonizes native type I collagen lattices. Infect Immun 72:3138-3146. (Pubitemid 38697734)
27. Yasui T, Tohno Y, Araki T (2004) Characterization of collagen orientation in human dermis by two-dimensional second-harmonic-generation polarimetry. J Biomed Opt 9:259-264.
28. Saidi IS, Jacques SL, Tittel FK (1995) Mie and Rayleigh modeling of visible-light scattering in neonatal skin. Appl Opt 34:7410-7418.
29. Goldstein SF, Charon NW (1990) Multiple-exposure photographic analysis of a motile spirochete. Proc Natl Acad Sci USA 87:4895-4899.
30. Teran J, Fauci L, Shelley M (2010) Viscoelastic fluid response can increase the speed and efficiency of a free swimmer. Phys Rev Lett 104:038101.
31. Markidou A, Shih WY, Shih W-H (2005) Soft-materials elastic and shear moduli measurements using piezoelectric cantilevers. Rev Sci Instrum 76:064302.
32. Berg HC, Turner L (1979) Movement of microorganisms in viscous environments. Nature 278:349-351. (Pubitemid 9124374)
33. Kimsey RB, Spielman A (1990) Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J Infect Dis 162:1205-1208. (Pubitemid 20353610)
34. Liu B, Powers TR, Breuer KS (2011) Force-free swimming of a model helical flagellum in viscoelastic fluids. Proc Natl Acad Sci USA 108:19516-19520.
35. Berg HC (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72:19-54.
36. Levin M, Papero M, Fish D (1997) Feeding density influences acquisition of Borrelia burgdorferi in larval Ixodes scapularis (Acari: Ixodidae). J Med Entomol 34:569-572. (Pubitemid 127460919)
37. Piesman J, Oliver JR, Sinsky RJ (1990) Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini). Am J Trop Med Hyg 42: 352-357. (Pubitemid 20137308)
38. Tilly K, Rosa PA, Stewart PE (2008) Biology of infection with Borrelia burgdorferi. Infect Dis Clin North Am 22:217-234, v. (Pubitemid 351608547)
39. Coleman JL, et al. (1997) Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111-1119. (Pubitemid 127678744)
40. Bockenstedt LK, et al. (1997) Borrelia burgdorferi strain-specific Osp C-mediated immunity in mice. Infect Immun 65:4661-4667. (Pubitemid 27463239)