Skip to main content
PMC home page
Brain Pathology logoLink to Brain Pathology
. 2006 Apr 5;11(4):432–438. doi: 10.1111/j.1750-3639.2001.tb00411.x

Evidence for Intraaxonal Spread of Listeria Monocytogenes from the Periphery to the Central Nervous System

Ellen‐Ann Antal 1,✉, Else Marit Løberg 1, Paula Bracht 3, Kjetil K Melby 2, Jan Mæhlen 1
PMCID: PMC8098618  PMID: 11556688

Abstract

Rhombencephalitis due to Listeria monocytogenes is characterized by progressive cranial nerve palsies and subacute inflammation in the brain stem. In this paper, we report observations made on mice infected with L. monocytogenes. Unilateral inoculation of bacteria into facial muscle, or peripheral parts of a cranial nerve, induced clinical and histological signs of mainly ipsilateral rhombencephalitis. Similarly, unilateral inoculation of bacteria into lower leg muscle or peripheral parts of sciatic nerve was followed by lumbar myelitis. In these animals, intraaxonal bacteria were seen in the sciatic nerve and its corresponding nerve roots ipsilateral to the bacterial application site. Development of myelitis was prevented by transsection of the sciatic nerve proximally to the hindleg inoculation site. Altogether, our results support the hypothesis that Listeria rhombencephalitis is caused by intraaxonal bacterial spread from peripheral sites to the central nervous system.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

References

  • 1. Allt G, Lawrenson JG (2000) The blood‐nerve barrier: Enzymes, transporters and receptors—a comparison with the blood‐brain barrier. Brain Res Bull 52:1–12. [DOI] [PubMed] [Google Scholar]
  • 2. Armstrong RW, Fung PC (1993) Brainstem encephalitis (rhombencephalitis) due to Listeria monocytogenes: case report and review. Clin Infect Dis 16:689–702. [DOI] [PubMed] [Google Scholar]
  • 3. Asahi O, Hosoda T, Akiyama Y (1957) Studies on the mechanism of infection of the brain with Listeria monocytogenes. Am J Vet Res 18:147–157. [PubMed] [Google Scholar]
  • 4. Berche P (1995) Bacteremia is required for invasion of the murine central nervous system by Listeria monocytogenes. Microb Pathogen 18:323–336. [DOI] [PubMed] [Google Scholar]
  • 5. Blanot S, Joly MM, Vilde F, Jaubert F, Clement O, Frija G, Berche P (1997) A gerbil model for rhombencephalitis due to Listeria monocytogenes. Microb Pathog 23:39–48. [DOI] [PubMed] [Google Scholar]
  • 6. Chakraborty T (1999) Molecular and cell biological aspects of infection by Listeria monocytogenes. Immuno-biology 201:155–163. [DOI] [PubMed] [Google Scholar]
  • 7. Charlton KM (1977) Spontaneous listeric encephalitis in sheep. Electron microscopic studies. Vet Pathol 14:429–434. [DOI] [PubMed] [Google Scholar]
  • 8. Charlton KM, Garcia MM (1977) Spontaneous listeric encephalitis in sheep. Light microscopic studies. Vet Pathol 14:297–313. [DOI] [PubMed] [Google Scholar]
  • 9. Cossart P, Kocks C (1994) The actin‐based motility of the facultative intracellular pathogen Listeria monocytogenes. Mol Microbiol 13:395–402. [DOI] [PubMed] [Google Scholar]
  • 10. Cudmore S, Cossart P, Griffiths G, Way M (1995) Actinbased motility of vaccinia virus. Nature 378:636–638. [DOI] [PubMed] [Google Scholar]
  • 11. Dramsi S, Cossart P (1998) Intracellular pathogens and the actin cytoskeleton. Annu Rev Cell Dev Biol 14:137–166. [DOI] [PubMed] [Google Scholar]
  • 12. Dramsi S, Levi S, Triller A, Cossart P (1998) Entry of Listeria monocytogenes into neurons occurs by cell‐to‐cell spread: an in vitro study. Infect Immun 66:4461–4468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13. Eck H (1957) Encephalomyelitis listeriaca apostomatosa. Schweiz Med Wochenschr 87:210–214. [PubMed] [Google Scholar]
  • 14. Fannon AM, Sherman DL, Ilyina‐Gragerova G, Brophy PJ, Friedrich VL Jr, Colman DR (1995) Novel E‐cadherin‐mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions [published erratum appears in J Cell Biol 1995;129:1721]. J Cell Biol 129:189–202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15. Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food‐borne pathogen [published erratum appears in Microbiol Rev 1991; 55:752]. Microbiol Rev 55:476–511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16. Forscher P, Lin CH, Thompson C (1992) Novel form of growth cone motility involving site‐directed actin filament assembly. Nature 357:515–518. [DOI] [PubMed] [Google Scholar]
  • 17. Gouin E, Gantelet H, Egile C, Lasa I, Ohayon H, Villiers V, Gounon P, Sansonetti PJ, Cossart P (1999) A comparative study of the actin‐based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112:1697–1708. [DOI] [PubMed] [Google Scholar]
  • 18. Hollenbeck PJ (1996) The pattern and mechanism of mitochondrial transport in axons. Front Biosci 1:91–102. [DOI] [PubMed] [Google Scholar]
  • 19. Ireton K, Cossart P (1997) Host‐pathogen interactions during entry and actin‐based movement of Listeria monocytogenes. Annu Rev Genet 31:113–138. [DOI] [PubMed] [Google Scholar]
  • 20. Kelly RM, Strick PL (2000) Rabies as a transneuronal tracer of circuits in the central nervous system. J Neurosci Methods 103:63–71. [DOI] [PubMed] [Google Scholar]
  • 21. Kocks C, Hellio R, Gounon P, Ohayon H, Cossart P (1993) Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J Cell Sci 105:699–710. [DOI] [PubMed] [Google Scholar]
  • 22. Kuypers HG, Ugolini G (1990) Viruses as transneuronal tracers. Trends Neurosci 13:71–75. [DOI] [PubMed] [Google Scholar]
  • 23. Lebrun M, Mengaud J, Ohayon H, Nato F, Cossart P (1996) Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Mol Microbiol 21:579–592. [DOI] [PubMed] [Google Scholar]
  • 24. Lorber B (1997) Listeriosis. Clin Infect Dis 24:1–11. [DOI] [PubMed] [Google Scholar]
  • 25. Low JC, Donachie W (1997) A review of Listeria monocytogenes and listeriosis. Vet J 153:9–29. [DOI] [PubMed] [Google Scholar]
  • 26. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P (1996) E‐cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923–932. [DOI] [PubMed] [Google Scholar]
  • 27. Otter A, Blakemore WF (1989) Observation on the presence of Listeria monocytogenes in axons. Acta Microbiol Hung 36:125–131. [PubMed] [Google Scholar]
  • 28. Parida SK, Domann E, Rohde M, Muller S, Darji A, Hain T, Wehland J, Chakraborty T (1998) Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol Microbiol 28:81–93. [DOI] [PubMed] [Google Scholar]
  • 29. Peters M, Hewicker‐Trautwein M (1994) Infection of murine fetal brain cell cultures with Listeria monocytogenes. Vet Microbiol 41:19–28. [DOI] [PubMed] [Google Scholar]
  • 30. Peters M, Hewicker‐Trautwein M (1996) Studies on the cell tropism of Listeria monocytogenes in ovine fetal brain cell cultures. Vet Microbiol 49:169–179. [DOI] [PubMed] [Google Scholar]
  • 31. Prats N, Briones V, Blanco MM, Altimira J, Dominguez L, Marco A (1992) Choroiditis and meningitis in experimental murine infection with Listeria monocytogenes. Eur J Clin Microbiol Infect Dis 11:744–747. [DOI] [PubMed] [Google Scholar]
  • 32. Robbins JR, Barth AI, Marquis H, De Hostos EL, Nelson WJ, Theriot JA (1999) Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. J Cell Biol 146:1333–1350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Sanger JM, Dold FG, Nanavati D, Sanger, JW (1998) Interactions of Listeria monocytogenes with infected host cells. Video supplement. Cell Motil Cytoskeleton 39:339–340. [PubMed] [Google Scholar]
  • 34. Shimamura K, Takahashi, T , Takeichi, M (1992) E‐cadherin expression in a particular subset of sensory neurons. Dev Biol 152:242–254. [DOI] [PubMed] [Google Scholar]
  • 35. Southwick FS, Purich, DL (1996) Intracellular pathogenesis of listeriosis. N Engl J Med 334:770–776. [DOI] [PubMed] [Google Scholar]
  • 36. Tilney LG, DeRosier DJ, Tilney MS (1992) How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J Cell Biol 118:71–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37. Tilney LG, DeRosier DJ, Weber A, Tilney MS (1992) How Listeria exploits host cell actin to form its own cytoskeleton. II. Nucleation, actin filament polarity, filament assembly, and evidence for a pointed end capper. J Cell Biol 118:83–93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Uldry PA, Kuntzer T, Bogousslavsky J, Regli F, Miklossy J, Bille J, et al. (1993) Early symptoms and outcome of Listeria monocytogenes rhombencephalitis: 14 adult cases. J Neurol 240:235–242. [DOI] [PubMed] [Google Scholar]
  • 39. Vandegraaff R, Borland, NA , Browning, JW (1981) An outbreak of listerial meningo‐encephalitis in sheep. Aust Vet J 57:94–96. [DOI] [PubMed] [Google Scholar]
  • 40. Wardrope DD, Macleod NS (1983) Outbreak of listeria meningoencephalitis in young lambs. Vet Rec 113:213–214. [DOI] [PubMed] [Google Scholar]

Articles from Brain Pathology are provided here courtesy of Wiley

RESOURCES