Anterograde axonal transport of the exogenous cellular isoform of prion protein in the chick visual system
Abstract
The cellular isoform of endogenous, newly synthesized prion protein (PrPc) can be transported by axons in the anterograde direction. To determine whether a mechanism exists for secreted PrPc to be internalized and then axonally transported, we analyzed internalization and anterograde axonal transport of radiolabeled recombinant PrPc after its intraocular injection in chick embryos. Internalization and axonal transport of exogenous PrPc to the midbrain by retinal ganglion cells (RGCs) is efficient, saturable and likely receptor-mediated. Ultrastructural quantitative localization of radiolabeled PrPc within RGC soma showed significant labeling of vesicular/endosomal compartments and much less labeling present over the Golgi apparatus and lysosomes, which indicates slow degradation of exogenous PrPc in this system. These data show that a mechanism exists to internalize a secreted form of PrPc and then to axonally transport such PrPc in an anterograde direction. This may provide an additional, novel mechanism for prion protein to spread among neurons.
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PrPC moves in anterograde and retrograde directions in nerves.
“Previous studies showed that PrPC moved in anterograde and retrograde directions in nerves”
From Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles (2011) · cites this paper as Butowt et al., 2006
Cites
A series of normal stages in the development of the chick embryo
Hamburger, V., & Hamilton, H. L. (1951) · Journal of Morphology · doi:10.1002/jmor.1050880104 · Cited by 12,254 · see citing works
The cellular prion protein binds copper in vivo
Brown, D. R., Qin, K., Herms, J., Madlung, A., Manson, J., Strome, R., Fraser, P., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W., et al. (1997) · Nature · doi:10.1038/37783 · Cited by 1,300 · see citing works
Self-citationScrapie prion protein contains a phosphatidylinositol glycolipid
Stahl, N. (1987) · Cell · doi:10.1016/0092-8674(87)90150-4 · Cited by 1,107 · see citing works
HIGH-RESOLUTION AUTORADIOGRAPHY
Caro, L. G., & van Tubergen, R. P. (1962) · The Journal of Cell Biology · doi:10.1083/jcb.15.2.173 · Cited by 1,073 · see citing works
Cells release prions in association with exosomes
Février, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., & Raposo, G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308413101 · Cited by 998 · see citing works
B lymphocytes and neuroinvasion
Brown, P. (1997) · Nature · doi:10.1038/37733 · Cited by 658 · see citing works
Copper Stimulates Endocytosis of the Prion Protein
Pauly, P. C., & Harris, D. A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.50.33107 · Cited by 591 · see citing works
Vey, M., Pilkuhn, S., Wille, H., Nixon, R. R., DeArmond, S. J., Smart, E. J., Anderson, R. G. W., Taraboulos, A., & Prusiner, S. B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14945 · Cited by 525 · see citing works
Normal prion protein has an activity like that of superoxide dismutase
Brown, D. R., Wong, B., Hafiz, F., Clive, C., Haswell, S. J., & Jones, I. M. (1999) · Biochemical Journal · doi:10.1042/bj3440001 · Cited by 524 · see citing works
Self-citationBorchelt, D., Scott, M., Taraboulos, A., et al. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.110.3.743 · Cited by 507 · see citing works
Nearly ubiquitous tissue distribution of the scrapie agent precursor protein
Bendheim, P. E., Brown, H. R., Rudelli, R. D., Scala, L. J., Goller, N. L., Wen, G. Y., Kascsak, R. J., Cashman, N. R., & Bolton, D. C. (1992) · Neurology · doi:10.1212/wnl.42.1.149 · Cited by 472 · see citing works
Prions prevent neuronal cell-line death
Kuwahara, C., Takeuchi, A. M., Nishimura, T., Haraguchi, K., Kubosaki, A., Matsumoto, Y., Saeki, K., Matsumoto, Y., Yokoyama, T., Itohara, S., et al. (1999) · Nature · doi:10.1038/22241 · Cited by 443 · see citing works
Scrapie prion proteins are synthesized in neurons.
Kretzschmar, H. A., Prusiner, S. B., Stowring, L., & DeArmond, S. J. (1986) · PubMed Central · Cited by 423 · see citing works
The development of the chick optic tectum. I. normal morphology and cytoarchitectonic development
LaVail, J. H., & Cowan, W. M. (1971) · Brain Research · doi:10.1016/0006-8993(71)90053-9 · Cited by 395 · see citing works
Cellular prion protein transduces neuroprotective signals
Chiarini, L. B., Freitas, A. R. O., Zanata, S. M., Brentani, R. R., Martins, V. R., & Linden, R. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf324 · Cited by 376 · see citing works
Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells
Caughey, B. W., Race, R., Ernst, D. R., Buchmeier, M. J., & Chesebro, B. W. (1989) · Journal of Virology · doi:10.1128/jvi.63.1.175-181.1989 · Cited by 343 · see citing works
The mechanism of internalization of glycosylphosphatidylinositol‐anchored prion protein
Sunyach, C., Jen, A., Deng, J., Fitzgerald, K. T., Frobert, Y., Grassi, J. J., McCaffrey, M., & Morris, R. J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg344 · Cited by 288 · see citing works
Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system
von Bartheld, C. S., Byers, M. R., Williams, R., & Bothwell, M. A. (1996) · Nature · doi:10.1038/379830a0 · Cited by 284 · see citing works
A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis
Schätzl, H. M., László, L., Holtzman, D. M., Tatzelt, J., DeArmond, S. J., Weiner, R. I., Mobley, W. C., & Prusiner, S. B. (1997) · Journal of Virology · doi:10.1128/jvi.71.11.8821-8831.1997 · Cited by 282 · see citing works
Molecular biology and pathogenesis of prion diseases
Prusiner, S. B. (1996) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)10063-3 · Cited by 280 · see citing works
Trafficking of prion proteins through a caveolae-mediated endosomal pathway
Peters, P. J., Mironov, A., Peretz, D., van Donselaar, E. G., Leclerc, E., Erpel, S., DeArmond, S. J., Burton, D. R., Williamson, R. A., Vey, M., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200304140 · Cited by 233 · see citing works
Processing of a cellular prion protein: identification of N- and C-terminal cleavage sites
Harris, D. A., Huber, M. T., van Dijken, P., et al. (1993) · Biochemistry · doi:10.1021/bi00055a003 · Cited by 217 · see citing works
Normal prion protein has an activity like that of superoxide dismutase
Brown, D. R., Wong, B., Hafiz, F., Clive, C., Haswell, S. J., & Jones, I. M. (1999) · Biochemical Journal · doi:10.1042/0264-6021:3440001 · Cited by 170 · see citing works
Self-citationRapid Prion Neuroinvasion following Tongue Infection
Bartz, J. C., Kincaid, A. E., & Bessen, R. A. (2002) · Journal of Virology · doi:10.1128/jvi.77.1.583-591.2003 · Cited by 168 · see citing works
Development of the visual system of the chick
Mey, J., & Thanos, S. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00022-3 · Cited by 165 · see citing works
Uptake and Neuritic Transport of Scrapie Prion Protein Coincident with Infection of Neuronal Cells
Magalhães, A. C., Baron, G. S., Lee, K. S., Steele‐Mortimer, O., Dorward, D. W., Prado, M. A. M., & Caughey, B. W. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0653-05.2005 · Cited by 158 · see citing works
Development of the Retinotectal Projection in the Chicken
Rager, G. H. (1980) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-642-67681-9 · Cited by 154 · see citing works
Dual Mechanisms for Shedding of the Cellular Prion Protein
Parkin, E. T., Watt, N. T., Turner, A. J., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312105200 · Cited by 136 · see citing works
Prion Glycoprotein: Structure, Dynamics, and Roles for the Sugars
Rudd, P. M., Wormald, M. R., Wing, D. R., et al. (2001) · Biochemistry · doi:10.1021/bi002625f · Cited by 133 · see citing works
Borchelt, D., Rogers, M. S., Stahl, N., et al. (1993) · Glycobiology · doi:10.1093/glycob/3.4.319 · Cited by 133 · see citing works
Borchelt, D. R., Koliatsos, V. E., Guarnieri, M., Pardo, C. A., Sisodia, S. S., & Price, D. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36683-8 · Cited by 132 · see citing works
Resolution of electron microscope autoradiography. IV. Application to analysis of autoradiographs.
Salpeter, M. M., McHenry, F. A., & Salpeter, E. E. (1978) · The Journal of Cell Biology · doi:10.1083/jcb.76.1.127 · Cited by 131 · see citing works
Graner, E., Mercadante, A. F., Zanata, S. M., Martins, V. R., Jay, D. G., & Brentani, H. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)02070-6 · Cited by 126 · see citing works
Rager, G. H. (1980) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-642-67681-9_1 · Cited by 114 · see citing works
Effects of oxidative stress on prion protein expression in pc12 cells
Brown, D. R., Schmidt, B., & Kretzschmar, H. A. (1997) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(97)00042-7 · Cited by 107 · see citing works
Self-citationIntercellular Transfer of the Cellular Prion Protein
Liu, T., Li, R., Pan, T., Liu, D., Petersen, R. B., Wong, B., Gambetti, P. L., & Sy, M. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207458200 · Cited by 106 · see citing works
[3] Assaying binding of nerve growth factor to cell surface receptors
Vale, R. D., & Shooter, E. M. (1985) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(85)09073-5 · Cited by 103 · see citing works
Exosomes: A Bubble Ride for Prions?
Février, B., Vilette, D., Laude, H., & Raposo, G. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.00247.x · Cited by 102 · see citing works
Fournier, J. G., Escaig-Haye, F., de Villemeur, T. B., & Robain, O. (1995) · PubMed · Cited by 101 · see citing works
Prion Protein Accumulation in Eyes of Patients with Sporadic and Variant Creutzfeldt-Jakob Disease
Head, M. W., Northcott, V., Rennison, K. A., et al. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.01-1273 · Cited by 96 · see citing works
Similar Turnover and Shedding of the Cellular Prion Protein in Primary Lymphoid and Neuronal Cells
Parizek, P., Roeckl, C., Weber, J., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107458200 · Cited by 96 · see citing works
Evidence for a secretory form of the cellular prion protein
Hay, B. A., Prusiner, S. B., & Lingappa, V. R. (1987) · Biochemistry · doi:10.1021/bi00399a014 · Cited by 96 · see citing works
Immunolocalization of the cellular prion protein in normal brain
Moya, K. L., Sal�s, N., H�ssig, R., Cr�minon, C., Grassi, J. J., & Giamberardino, L. D. (2000) · Microscopy Research and Technique · doi:10.1002/1097-0029(20000701)50:1 · Cited by 95 · see citing works
A marked disparity between the expression of prion protein and its message by neurones of the CNS
Ford, M. J., Burton, L., Li, H., Graham, C. H., Frobert, Y., Grassi, J. J., Hall, S. M., & Morris, R. J. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00603-0 · Cited by 95 · see citing works
Developmental expression of the cellular prion protein in elongating axons
Salès, N., Hässig, R., Rodolfo, K., Giamberardino, L. D., Traiffort, É., Ruat, M., Frétier, P., & Moya, K. L. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01953.x · Cited by 92 · see citing works
Rind, H. B., Butowt, R., & von Bartheld, C. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4322-04.2005 · Cited by 91 · see citing works
Self-citationTagliavini, F., Prelli, F., Porro, M., et al. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(05)80038-5 · Cited by 89 · see citing works
Localization of the mRNA for a chicken prion protein by in situ hybridization.
Harris, D. A., Lele, P., & Snider, W. D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.9.4309 · Cited by 89 · see citing works
PrPc on the road: trafficking of the cellular prion protein
Prado, M. A. M., Alves‐Silva, J., Magalhães, A. C., Prado, V. F., Linden, R., Martins, V. R., & Brentani, R. R. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02199.x · Cited by 84 · see citing works
Butowt, R., & von Bartheld, C. S. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-22-08915.2001 · Cited by 83 · see citing works
Self-citationRole of the prion protein in copper turnover in astrocytes
Brown, D. R. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.11.009 · Cited by 75 · see citing works
Self-citationHippocampal synaptic plasticity in mice devoid of cellular prion protein
Maglio, L. E., Pérez, M. F., Martins, V. R., Brentani, H., & Ramírez, O. A. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.08.004 · Cited by 73 · see citing works
Barmada, S. J., Piccardo, P., Yamaguchi, K., Ghetti, B. F., & Harris, D. A. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.05.005 · Cited by 70 · see citing works
Künzi, V., Glatzel, M., Nakano, M. Y., Greber, U. F., LEUVEN, F. V., & Aguzzi, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07471.2002 · Cited by 67 · see citing works
Enhanced detection and retrograde axonal transport of PrP<sup>c</sup> in peripheral nerve
Moya, K. L., Hässig, R., Créminon, C., Laffont, I., & Di Giamberardino, L. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02150.x · Cited by 58 · see citing works
Kiachopoulos, S., Heske, J., Tatzelt, J., & Winklhofer, K. F. (2004) · Traffic · doi:10.1111/j.1398-9219.2004.00185.x · Cited by 50 · see citing works
Neuronal activity-dependent membrane traffic at the neuromuscular junction
MENA, F., Roux, S., Bénichou, J.-C., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052023599 · Cited by 48 · see citing works
A novel cellular prion protein isoform present in rapid anterograde axonal transport
Rodolfo, K., Hässig, R., Moya, K. L., Frobert, Y., Grassi, J. J., & Giamberardino, L. D. (1999) · Neuroreport · doi:10.1097/00001756-199911260-00032 · Cited by 46 · see citing works
Margolis, T. P., Marchand, C. M., Kistler, H. B., et al. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.89.1.152 · Cited by 45 · see citing works
Butowt, R., & von Bartheld, C. S. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.02.004 · Cited by 40 · see citing works
Self-citationTracing with Radiolabeled Neurotrophins
von Bartheld, C. S. (2003) · Humana Press eBooks · doi:10.1385/1-59259-060-8:195 · Cited by 37 · see citing works
In situ hybridization analysis of PrP mRNA in human CNS tissues
McLennan, N. F., Rennison, K. A., Bell, J. E., et al. (2001) · Neuropathology and Applied Neurobiology · doi:10.1046/j.0305-1846.2001.00343.x · Cited by 34 · see citing works
Williams, C., & McLoon, S. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-02-00445.1991 · Cited by 32 · see citing works
Borchelt, D., Scott, M. J., Taraboulos, A., et al. (1990) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199005000-00156 · Cited by 26 · see citing works
Syrian hamster prion protein (PrPC) is expressed in photoreceptor cells of the adult retina
Chishti, M. A., Strome, R., Carlson, G. A., & Westaway, D. A. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00669-1 · Cited by 22 · see citing works
Displaced ganglion cells in the chick retina
Prada, F. A., Chmielewski, C. E., Dorado, M. E., et al. (1989) · Neuroscience Research · doi:10.1016/0168-0102(89)90025-4 · Cited by 21 · see citing works
Expression of the prion protein in the rat forebrain – an immunohistochemical study
Verghese-Nikolakaki, S., Michaloudi, H. C., Polymenidou, M., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00563-7 · Cited by 21 · see citing works
Butowt, R., Jeffrey, P. L., & von Bartheld, C. S. (2000) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00149-1 · Cited by 20 · see citing works
Self-citationGremo, F., & Marchisio, P. (1975) · Cell and Tissue Research · doi:10.1007/bf00220000 · Cited by 16 · see citing works
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Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles
Encalada, S. E., Szpankowski, L., Xia, C.-H., & Goldstein, L. S. B. (2011) · Cell · doi:10.1016/j.cell.2011.01.021 · Cited by 206 · see citing works
- Authors
- Butowt, R., Abdelraheim, S., Brown, D. R., & von Bartheld, C. S.
- Affiliations
- University of Bath (GB)
- ORCID
- Brown, David R.
- Venue
- Molecular and Cellular Neuroscience
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 31
- Issue
- 1
- Pages
- 97-108
- ISSN
- 1044-7431 (ISSN-L)
- OpenAlex
- W2008850684
- Cited by
- 12
- References
- 69
- Citations by year
- 2021: 1 · 2020: 1 · 2014: 1
- FWCI
- 0.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular and Cellular Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r03ey014405-03)
- National Eye Institute (EY14405, R01EY012841, EY 12841)
- National Institute of Neurological Disorders and Stroke (NS 47216, R21NS047216)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Prion Diseases and Protein Misfolding
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- prion protein, anterograde axonal transport, retinal ganglion cells, chick embryo, retinohypothalamic pathway, receptor-mediated internalization, vesicular compartments, endosomal degradation, visual system
- MeSH terms
- Animals, Axons, Axonal Transport, Chick Embryo, Prions, Recombinant Proteins, Retina, Retinal Ganglion Cells, Vision, Ocular
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