A hitchhiker's guide to the nervous system: The complex journey of viruses and toxins

Nature Reviews Microbiology

Volumn 8, Issue 9, 2010, Pages 645-655

  Salinas, Sara ^a,b   Schiavo, Giampietro ^c   Kremer, Eric J ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BACTERIAL TOXIN; LENTIVIRUS VECTOR; TOXIN; UNCLASSIFIED DRUG; VIRUS TOXIN; VIRUS VECTOR;

ADENO ASSOCIATED VIRUS; BLOOD BRAIN BARRIER; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM INFECTION; CLOSTRIDIUM; ENDOSOME; GENE TRANSFER; HERPES SIMPLEX VIRUS; HUMAN; NERVE CELL; NERVE FIBER TRANSPORT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VIRUS;

AXONAL TRANSPORT; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL TOXINS; BLOOD-BRAIN BARRIER; NERVOUS SYSTEM; VIRUS PHYSIOLOGICAL PHENOMENA;

BACTERIA (MICROORGANISMS);

EID: 77955597073     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2395     Document Type: Review

References (121)

1. Resnick, L. et al. Intra-blood-brain-barrier synthesis of HTLV-III-specific IgG in patients with neurologic symptoms associated with AIDS or AIDS-related complex. N. Engl. J. Med. 313, 1498-1504 (1985).
2. Caleo, M. & Schiavo, G. Central effects of tetanus and botulinum neurotoxins. Toxicon 54, 593-599 (2009).
3. Woldehiwet, Z. Rabies: recent developments. Res. Vet. Sci. 73, 17-25 (2002).
4. Brahic, M., Bureau, J. F. & Michiels, T. The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu. Rev. Microbiol. 59, 279-298 (2005).
5. Hans, A. et al. Persistent, noncytolytic infection of neurons by Borna disease virus interferes with ERK 1/2 signaling and abrogates BDNF-induced synaptogenesis. FASEB J. 18, 863-865 (2004).
6. Mattson, M. P. Infectious agents and age-related neurodegenerative disorders. Ageing Res. Rev. 3, 105-120 (2004).
7. Ravits, J. Sporadic amyotrophic lateral sclerosis: a hypothesis of persistent (non-lytic) enteroviral infection. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 6, 77-87 (2005).
8. Jang, H., Boltz, D. A., Webster, R. G. & Smeyne, R. J. Viral parkinsonism. Biochim. Biophys. Acta 1792, 714-721 (2009).
9. Jang, H. et al. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl Acad. Sci. USA 106, 14063-14068 (2009).
10. Berth, S. H., Leopold, P. L. & Morfini, G. N. Virusinduced neuronal dysfunction and degeneration. Front. Biosci. 14, 5239-5259 (2009).
11. Barnes, A. P. & Polleux, F. Establishment of axondendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381 (2009).
12. Horton, A. C. & Ehlers, M. D. Neuronal polarity and trafficking. Neuron 40, 277-295 (2003).
13. Conde, C. & Caceres, A. Microtubule assembly, organization and dynamics in axons and dendrites. Nature Rev. Neurosci. 10, 319-332 (2009).
14. Salinas, S., Bilsland, L. G. & Schiavo, G. Molecular landmarks along the axonal route: axonal transport in health and disease. Curr. Opin. Cell Biol. 20, 445-453 (2008).
15. Muller, M. J., Klumpp, S. & Lipowsky, R. Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc. Natl Acad. Sci. USA 105, 4609-4614 (2008).
16. Song, A. H. et al. A selective filter for cytoplasmic transport at the axon initial segment. Cell 136, 1148-1160 (2009).
17. Martin, K. C. et al. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-938 (1997).
18. Hanz, S. et al. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104 (2003).
19. Lin, A. C. & Holt, C. E. Function and regulation of local axonal translation. Curr. Opin. Neurobiol. 18, 60-68 (2008).
20. Cosker, K. E., Courchesne, S. L. & Segal, R. A. Action in the axon: generation and transport of signaling endosomes. Curr. Opin. Neurobiol. 18, 270-275 (2008).
21. Ibanez, C. F. Message in a bottle: long-range retrograde signaling in the nervous system. Trends Cell Biol. 17, 519-528 (2007).
22. De Vos, K. J., Grierson, A. J., Ackerley, S. & Miller, C. C. Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 31, 151-173 (2008).
23. Racaniello, V. R. One hundred years of poliovirus pathogenesis. Virology 344, 9-16 (2006).
24. Finke, S. & Conzelmann, K. K. Replication strategies of rabies virus. Virus Res. 111, 120-131 (2005).
25. Diefenbach, R. J., Miranda-Saksena, M., Douglas, M. W. & Cunningham, A. L. Transport and egress of herpes simplex virus in neurons. Rev. Med. Virol. 18, 35-51 (2008).
26. Lalli, G., Bohnert, S., Deinhardt, K., Verastegui, C. &Schiavo, G. The journey of tetanus and botulinum neurotoxins in neurons. Trends Microbiol. 11, 431-437 (2003).
27. Samuel, M. A., Wang, H., Siddharthan, V., Morrey, J. D. & Diamond, M. S. Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc. Natl Acad. Sci. USA 104, 17140-17145 (2007).
28. Wang, H., Siddharthan, V., Hall, J. O. & Morrey, J. D. West Nile virus preferentially transports along motor neuron axons after sciatic nerve injection of hamsters. J. Neurovirol. 15, 293-299 (2009).
29. Roussarie, J. P., Ruffie, C. & Brahic, M. The role of myelin in Theiler's virus persistence in the central nervous system. PLoS Pathog 3, e23 (2007).
30. Young, V. A. & Rall, G. F. Making it to the synapse: measles virus spread in and among neurons. Curr. Top. Microbiol. Immunol. 330, 3-30 (2009)
31. De la Torre, J. C. Bornavirus and the brain. J. Infect. Dis. 186, S241-S247 (2002).
32. Chen, C. S. et al. Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J. Virol. 81, 8996-9003 (2007).
33. Antonucci, F., Rossi, C., Gianfranceschi, L., Rossetto, O. & Caleo, M. Long-distance retrograde effects of botulinum neurotoxin A. J. Neurosci. 28, 3689-3696 (2008).
34. Rudd, P. A., Cattaneo, R. & von Messling, V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J. Virol. 80, 9361-9370 (2006).
35. Soudais, C., Laplace-Builhe, C., Kissa, K. &Kremer, E. J. Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB J. 15, 2283-2285 (2001).
36. Kremer, E. J. Gene transfer to the central nervous system: current state of the art of the viral vectors. Curr. Genomics 6, 13-39 (2005).
37. Callaway, E. M. Transneuronal circuit tracing with neurotropic viruses. Curr. Opin. Neurobiol. 18, 617-623 (2008).
38. Bilsland, L. G. & Schiavo, G. in The New Encyclopedia of Neuroscience (ed. Squire, L. R.) 1209-1216 (Academic Press, Oxford, UK, 2008).
39. Cossart, P., Boquet, P., Normark, S. & Rappuoli, R. Cellular microbiology emerging. Science 271, 315-316 (1996).
40. Greber, U. F. & Way, M. A superhighway to virus infection. Cell 124, 741-754 (2006).
41. Dietzschold, B., Schnell, M. & Koprowski, H. Pathogenesis of rabies. Curr. Top. Microbiol. Immunol. 292, 45-56 (2005).
42. Carbone, K. M., Trapp, B. D., Griffin, J. W., Duchala, C. S. & Narayan, O. Astrocytes and Schwann cells are virus-host cells in the nervous system of rats with borna disease. J. Neuropathol. Exp. Neurol. 48, 631-644 (1989).
43. Ohka, S., Yang, W. X., Terada, E., Iwasaki, K. &Nomoto, A. Retrograde transport of intact poliovirus through the axon via the fast transport system. Virology 250, 67-75 (1998).
44. Lewis, P., Fu, Y. & Lentz, T. L. Rabies virus entry at the neuromuscular junction in nerve-muscle cocultures. Muscle Nerve 23, 720-730 (2000).
45. Salinas, S. et al. CAR-associated vesicular transport of an adenovirus in motor neuron axons. PLoS Pathog 5, e1000442 (2009).
46. Ugolini, G. Use of rabies virus as a transneuronal tracer of neuronal connections: implications for the understanding of rabies pathogenesis. Dev. Biol. (Basel) 131, 493-506 (2008).
47. Shupliakov, O. The synaptic vesicle cluster: a source of endocytic proteins during neurotransmitter release. Neuroscience 158, 204-210 (2009).
48. Desplanques, A. S., Nauwynck, H. J., Vercauteren, D., Geens, T. & Favoreel, H. W. Plasma membrane cholesterol is required for efficient pseudorabies virus entry. Virology 376, 339-345 (2008).
49. Herreros, J., Ng, T. & Schiavo, G. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 12, 2947-2960 (2001).
50. Spear, P. G. & Longnecker, R. Herpesvirus entry: an update. J. Virol. 77, 10179-10185 (2003).
51. Spear, P. G., Eisenberg, R. J. & Cohen, G. H. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275, 1-8 (2000).
52. Richart, S. M. et al. Entry of herpes simplex virus type 1 into primary sensory neurons in vitro is mediated by nectin-1/HveC. J. Virol. 77, 3307-3311 (2003).
53. Mata, M., Zhang, M., Hu, X. & Fink, D. J. HveC (nectin-1) is expressed at high levels in sensory neurons, but not in motor neurons, of the rat peripheral nervous system. J. Neurovirol. 7, 476-480 (2001).
54. Ohka, S. et al. Receptor (CD155)-dependent endocytosis of poliovirus and retrograde axonal transport of the endosome. J. Virol. 78, 7186-7198 (2004).
55. Lafon, M. Rabies virus receptors. J. Neurovirol. 11, 82-87 (2005).
56. Langevin, C., Jaaro, H., Bressanelli, S., Fainzilber, M. & Tuffereau, C. Rabies virus glycoprotein (RVG) is a trimeric ligand for the N-terminal cysteine-rich domain of the mammalian p75 neurotrophin receptor. J. Biol. Chem. 277, 37655-37662 (2002).
57. Wisco, D. et al. Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol. 162, 1317-1328 (2003).
58. Ascano, M., Richmond, A., Borden, P. & Kuruvilla, R. Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J. Neurosci. 29, 11674-11685 (2009).
59. Dubberke, E. R. et al. Acute meningoencephalitis caused by adenovirus serotype J. Neurovirol. 12, 235-240 (2006).
60. Berger, J. R., Chumley, W., Pittman, T., Given, C. &Nuovo, G. Persistent Coxsackie B encephalitis: Report of a case and review of the literature. J. Neurovirol. 12, 511-516 (2006).
61. Gruenberg, J. & Van Der Goot, F. G. Mechanisms of pathogen entry through the endosomal compartments. Nature Rev. Mol. Cell Biol. 7, 495-504 (2006).
62. Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902 (2009).
63. Wilson, J. M. et al. EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts. Mol. Biol. Cell 11, 2657-2671 (2000).
64. Smith, S. M., Renden, R. & von Gersdorff, H. Synaptic vesicle endocytosis: fast and slow modes of membrane retrieval. Trends Neurosci. 31, 559-568 (2008).
65. Darcy, K. J., Staras, K., Collinson, L. M. & Goda, Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nature Neurosci. 9, 315-321 (2006).
66. Deinhardt, K. et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52, 293-305 (2006).
67. Ohka, S. et al. Receptor-dependent and-independent axonal retrograde transport of poliovirus in motor neurons. J. Virol. 83, 4995-5004 (2009).
68. Deinhardt, K., Reversi, A., Berninghausen, O., Hopkins, C. R. & Schiavo, G. Neurotrophins redirect p75NTR from a clathrin-independent to a clathrindependent endocytic pathway coupled to axonal transport. Traffic 8, 1736-1749 (2007).
69. Nicola, A. V., Hou, J., Major, E. O. & Straus, S. E. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J. Virol. 79, 7609-7616 (2005).
70. Roche, S. & Gaudin, Y. Evidence that rabies virus forms different kinds of fusion machines with different pH thresholds for fusion. J. Virol. 78, 8746-8752 (2004).
71. Klingen, Y., Conzelmann, K. K. & Finke, S. Doublelabeled rabies virus: live tracking of enveloped virus transport. J. Virol. 82, 237-245 (2008).
72. Leopold, P. L. & Crystal, R. G. Intracellular trafficking of adenovirus: many means to many ends. Adv. Drug Deliv. Rev. 59, 810-821 (2007).
73. Meier, O. & Greber, U. F. Adenovirus endocytosis. J. Gene Med. 5, 451-462 (2003).
74. Bremner, K. H. et al. Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe 6, 523-535 (2009).
75. Sodeik, B. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8, 465-472 (2000).
76. Sodeik, B., Ebersold, M. & Helenius, A. Microtubulemediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136, 1007-1021 (1997).
77. Bearer, E. L. et al. Squid axoplasm supports the retrograde axonal transport of herpes simplex virus. Biol. Bull. 197, 257-258 (1999).
78. Bearer, E. L., Breakefield, X. O., Schuback, D., Reese, T. S. & LaVail, J. H. Retrograde axonal transport of herpes simplex virus: evidence for a single mechanism and a role for tegument. Proc. Natl Acad. Sci. USA 97, 8146-8150 (2000).
79. Dohner, K. et al. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13, 2795-2809 (2002).
80. Ye, G. J., Vaughan, K. T., Vallee, R. B. & Roizman, B. The herpes simplex virus 1 UL34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane. J. Virol. 74, 1355-1363 (2000).
81. Martinez-Moreno, M. et al. Recognition of novel viral sequences that associate with the dynein light chain LC8 identified through a pepscan technique. FEBS Lett. 544, 262-267 (2003).
82. Douglas, M. W. et al. Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J. Biol. Chem. 279, 28522-28530 (2004).
83. Antinone, S. E. et al. The herpesvirus capsid surface protein, VP26, and the majority of the tegument proteins are dispensable for capsid transport toward the nucleus. J. Virol. 80, 5494-5498 (2006).
84. Dohner, K., Radtke, K., Schmidt, S. & Sodeik, B. Eclipse phase of herpes simplex virus type 1 infection: efficient dynein-mediated capsid transport without the small capsid protein VP26. J. Virol. 80, 8211-8224 (2006).
85. Antinone, S. E. & Smith, G. A. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J. Virol. 84, 1504-1512 (2009).
86. Diefenbach, R. J. et al. Herpes simplex virus tegument protein US11 interacts with conventional kinesin heavy chain. J. Virol. 76, 3282-3291 (2002).
87. Smith, G. A., Gross, S. P. & Enquist, L. W. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl Acad. Sci. USA 98, 3466-3470 (2001).
88. Smith, G. A., Pomeranz, L., Gross, S. P. & Enquist, L. W. Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl Acad. Sci. USA 101, 16034-16039 (2004).
89. Luxton, G. W. et al. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl Acad. Sci. USA 102, 5832-5837 (2005).
90. Raux, H., Flamand, A. & Blondel, D. Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74, 10212-10216 (2000).
91. Mebatsion, T. Extensive attenuation of rabies virus by simultaneously modifying the dynein light chain binding site in the P protein and replacing Arg333 in the G protein. J. Virol. 75, 11496-11502 (2001).
92. Tan, G. S., Preuss, M. A., Williams, J. C. & Schnell, M. J. The dynein light chain 8 binding motif of rabies virus phosphoprotein promotes efficient viral transcription. Proc. Natl Acad. Sci. USA 104, 7229-7234 (2007).
93. Mazarakis, N. D. et al. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum. Mol. Genet. 10, 2109-2121 (2001).
94. Mueller, S., Cao, X., Welker, R. & Wimmer, E. Interaction of the poliovirus receptor CD155 with the dynein light chain Tctex-1 and its implication for poliovirus pathogenesis. J. Biol. Chem. 277, 7897-7904 (2002).
95. Lalli, G. & Schiavo, G. Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. J. Cell Biol. 156, 233-239 (2002).
96. Bohnert, S. & Schiavo, G. Tetanus toxin is transported in a novel neuronal compartment characterized by a specialized pH regulation. J. Biol. Chem. 280, 42336-42344 (2005).
97. Greber, U. F., Willetts, M., Webster, P. & Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486 (1993).
98. Haik, S., Faucheux, B. A. & Hauw, J. J. Brain targeting through the autonomous nervous system: lessons from prion diseases. Trends Mol. Med. 10, 107-112 (2004).
99. Bartz, J. C., Kincaid, A. E. & Bessen, R. A. Rapid prion neuroinvasion following tongue infection. J. Virol. 77, 583-591 (2003).
100. Ermolayev, V. et al. Impaired axonal transport in motor neurons correlates with clinical prion disease. PLoS Pathog 5, e1000558 (2009).
101. Haughey, N. J. & Mattson, M. P. Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J. Acquir. Immune Defic. Syndr. 31, S55-S61 (2002).
102. Ahmed, F., MacArthur, L., De Bernardi, M. A. &Mocchetti, I. Retrograde and anterograde transport of HIV protein gp120 in the nervous system. Brain Behav. Immun. 23, 355-364 (2009).
103. Bachis, A., Aden, S. A., Nosheny, R. L., Andrews, P. M. & Mocchetti, I. Axonal transport of human immunodeficiency virus type 1 envelope protein glycoprotein 120 is found in association with neuronal apoptosis. J. Neurosci. 26, 6771-6780 (2006).
104. Chauhan, A. et al. Intracellular human immunodeficiency virus Tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J. Biol. Chem. 278, 13512-13519 (2003).
105. Hendricks, A. G. et al. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol. 20, 697-702 (2010).
106. Knipe, D. M. & Cliffe, A. Chromatin control of herpes simplex virus lytic and latent infection. Nature Rev. Microbiol. 6, 211-221 (2008).
107. Del Rio, T., Ch'ng, T. H., Flood, E. A., Gross, S. P. &Enquist, L. W. Heterogeneity of a fluorescent tegument component in single pseudorabies virus virions and enveloped axonal assemblies. J. Virol. 79, 3903-3919 (2005).
108. Antinone, S. E. & Smith, G. A. Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J. Virol. 80, 11235-11240 (2006).
109. Maresch, C. et al. Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons. J. Virol. 84, 5528-5539 (2010).
110. Enquist, L. W., Tomishima, M. J., Gross, S. & Smith, G. A. Directional spread of an alpha-herpesvirus in the nervous system. Vet. Microbiol. 86, 5-16 (2002).
111. Holland, D. J., Miranda-Saksena, M., Boadle, R. A., Armati, P. & Cunningham, A. L. Anterograde transport of herpes simplex virus proteins in axons of peripheral human fetal neurons: an immunoelectron microscopy study. J. Virol. 73, 8503-8511 (1999).
112. McGraw, H. M. & Friedman, H. M. Herpes simplex virus type 1 glycoprotein E mediates retrograde spread from epithelial cells to neurites. J. Virol. 83, 4791-4799 (2009).
113. McGraw, H. M., Awasthi, S., Wojcechowskyj, J. A. &Friedman, H. M. Anterograde spread of herpes simplex virus type 1 requires glycoprotein E and glycoprotein I but not Us9. J. Virol. 83, 8315-8326 (2009).
114. Menager, P. et al. Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog 5, e1000315 (2009).
115. Ch'ng, T. H. & Enquist L. W. Neuron-to-cell spread of pseudorabies virus in a compartmented neuronal culture system. J. Virol. 79 10875-10889 (2005).
116. Horton, A. C. et al. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771 (2005).
117. Merianda, T. T. et al. A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol. Cell Neurosci. 40, 128-142 (2009).
118. Miranda-Saksena, M., Armati, P., Boadle, R. A., Holland, D. J. & Cunningham, A. L. Anterograde transport of herpes simplex virus type 1 in cultured, dissociated human and rat dorsal root ganglion neurons. J. Virol. 74, 1827-1839 (2000).
119. Strunze, S., Trotman, L. C., Boucke, K. & Greber, U. F. Nuclear targeting of adenovirus type 2 requires CRM1-mediated nuclear export. Mol. Biol. Cell 16, 2999-3009 (2005).
120. Gazzola, M. et al. A stochastic model for microtubule motors describes the in vivo cytoplasmic transport of human adenovirus. PLoS Comput. Biol. 5, e1000623 (2009).
121. Kam, N., Pilpel, Y. & Fainzilber, M. Can molecular motors drive distance measurements in injured neurons? PLoS Comput. Biol. 5, e1000477 (2009).