The cellular prion protein in multiple sclerosis: A potential target for neurotherapeutics?

Steinman L., Martin R., Bernard C., Conlon P., Oksenberg J. R., Multiple sclerosis: deeper understanding of its pathogenesis reveals new targets for therapy, Annu. Rev. Neurosci., 2002, 25, 491–505 Lucchinetti C. F., Brueck W., Rodriguez M., Lassmann H., Multiple sclerosis: lessons from neuropathology, Semin. Neurol., 1998, 18, 337–349 Villoslada P., Barcellos L. F., Oksenberg J. R., Chromosome 7q21–22 and multiple sclerosis, J. Neuroimmunol., 2004, 150, 1–2 Prat A., Antel J., Pathogenesis of multiple sclerosis, Curr. Opin. Neurol., 2005, 18, 225–230 Trapp B. D., Bö L., Mörk S., Chang A., Pathogenesis of tissue injury in MS lesions, J. Neuroimmunol., 1999, 98, 49–56 Tran E. H., Hoekstra K., van Rooijen N., Dijkstra C. D., Owens T., Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice, J. Immunol., 1998, 161, 3767–3775 Lassmann H., Bruck W, Lucchinetti C., Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy, Trends Mol. Med., 2001, 7, 115–121 Cifelli A., Arridge M., Jezzard P., Esiri M. M., Palace J., Matthews P. M., Thalamic neurodegeneration in multiple sclerosis, Ann. Neurol., 2002, 52, 650–653 Sospedra M., Martin R., Immunology of multiple sclerosis, Annu. Rev. Immunol., 2005, 23, 683–747 Rao S. M., Leo G. J., Bernardin L., Unverzagt F., Cognitive dysfunction in multiple sclerosis, I. Frequency, patterns, and prediction, Neurology, 1991, 41, 685–691 Ferguson B., Matyszak M. K., Esiri M. M., Perry V. H., Axonal damage in acute multiple sclerosis lesions, Brain, 1997, 120, 393–399 Gehrmann J., Banati R. B., Cuzner M. L., Kreutzberg G. W., Newcombe J., Amyloid precursor protein (APP) expression in multiple sclerosis lesions, Glia, 1995, 15, 141–151 Trapp B. D., Peterson J., Ransohoff R. M., Rudick R., Mörk S., Bö L., Axonal transection in the lesions of multiple sclerosis, N. Engl. J. Med., 1998, 338, 278–285 Moser M., Colello R. J., Pott U., Oesch B., Developmental expression of the prion protein gene in glial cells, Neuron, 1995, 14, 509–517 Lledo P. M., Alonso M., Grubb M. S., Adult neurogenesis and functional plasticity in neuronal circuits, Nat. Rev. Neurosci., 2006, 7, 179–193 Peters A., Palay S. L., The morphology of synapses, J. Neurocytol., 1996, 25, 687–700 Hoek R. M., Ruuls S. R., Murphy C. A., Wright G. J., Goddard R., Zurawski S. M. et al., Down-regulation of the macrophage lineage through interaction with OX2 (CD200), Science, 2000, 290, 1768–1771 Sofroniew M. V., Reactive astrocytes in neural repair and protection. Neuroscientist, 2005, 11, 400–407 Nguyen M. D., Julien J. P., Rivest S., Innate immunity: the missing link in neuroprotection and neurodegeneration?, Nat. Rev. Neurosci., 2002, 3, 216–227 Martino G., How the brain repairs itself: new therapeutic strategies in inflammatory and degenerative CNS disorders, Lancet Neurol., 2004, 3, 372–378 Butzkueven H., Zhang J. G., Soilu-Hanninen M., Hochrein H., Chionh F., Shipkam K. A. et al., LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival, Nat. Med., 2002, 8, 613–619 Zanata S. M., Lopes M. H., Mercadante A. F., Hajj G. N., Chiarini L. B., Nomizo R. et al., Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection, EMBO J., 2002, 21, 3307–3316 Lee J. W., Juliano R., Mitogenic signal transduction by integrin- and growth factor receptor-mediated pathways, Mol. Cells, 2004, 17, 188–202 Serafini B., Rosicarelli B., Magliozzi R., Stigliano E., Capello E., Mancardi G. L. et al., Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells, J. Neuropathol. Exp. Neurol., 2006, 65, 124–141 Frohman E. M., Racke M. K., Raine C. S., Multiple sclerosis — the plaque and its pathogenesis, N. Engl. J. Med., 2006, 354, 942–955 Carson M. J., Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis, Glia, 2002, 40, 218–231 Huseby E. S., Liggitt D., Brabb T., Schnabel B., Ohlén C., Goverman J., A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis, J. Exp. Med., 2001, 194, 669–676 Monson N. L., Brezinschek H. P., Brezinschek R. I., Mobley A., Vaughan G. K., Frohman E. M. et al., Receptor revision and atypical mutational characteristics in clonally expanded B cells from the cerebrospinal fluid of recently diagnosed multiple sclerosis patients, J. Neuroimmunol., 2005, 158, 170–181 Pashenkov M., Teleshova N., Link H., Inflammation in the central nervous system: the role for dendritic cells, Brain Pathol., 2003, 13, 23–33 Tailor P., Tamura T., Ozato K., IRF family proteins and type I interferon induction in dendritic cells, Cell Res., 2006, 16, 134–140 Tsutsui S., Hahn J. N., Johnson T. A., Ali Z., Jirik F. R., Absence of the cellular prion protein exacerbates and prolongs neuroinflammation in experimental autoimmune encephalomyelitis, Am. J. Pathol., 2008, 173, 1029–1041 Hu W., Nessler S., Hemmer B., Eagar T. N., Kane L. P., Leliveld S. R. et al., Pharmacological prion protein silencing accelerates central nervous system autoimmune disease via T cell receptor signalling, Brain, 133, 375–388 Burthem J., Urban B., Pain A., Roberts D. J., The normal cellular prion protein is strongly expressed by myeloid dendritic cells, Blood, 2001, 98, 3733–3738 Krebs B., Dorner-Ciossek C., Schumalzbauer R., Vassalo N., Herms J., Kretzschmar H. A., Prion protein induced signaling cascades in monocytes, Biochem. Biophys. Res. Commun., 2006, 340, 13–22 Brown D. R., Besinger A., Herms J. W., Kretzschmar H. A., Microglial expression of the prion protein, Neuroreport, 1998, 9, 1425–1429 Linden R., Martins V. R., Prado M. A., Cammarota M., Izquierdo I., Brentani R. R., Physiology of the prion protein, Physiol. Rev., 2008, 88, 673–728 de Almeida C. J., Chiarini L. B., da Silva J. P., E Silva P. M., Martins M. A., Linden R., The cellular prion protein modulates phagocytosis and inflammatory response, J. Leukoc. Biol., 2005, 77, 238–246 Nelson P. T., Soma L. A., Lavi E., Microglia in diseases of the central nervous system, Ann. Med., 2002, 34, 491–500 Antony J. M., Paquin A., Nutt S. L., Kaplan D. R., Miller F. D., Endogenous microglia regulate development of embryonic cortical precursor cells, J. Neurosci. Res., 89, 286–298 Ford M. J., Burton L. J., Morris R. J., Hall S. M., Selective expression of prion protein in peripheral tissues of the adult mouse, Neuroscience, 2002, 113, 177–192 Bradford B. M., Tuzi N. L., Feltri M. L., McCorquodale C., Cancellotti E., Manson J. C., Dramatic reduction of PrP C level and glycosylation in peripheral nerves following PrP knock-out from Schwann cells does not prevent transmissible spongiform encephalopathy neuroinvasion, J. Neurosci., 2009, 29, 15445–15454 Follet J., Lemaire-Vieille C., Blanquet-Grossard F., Podevin-Dimster V., Lehmann S., Chauvin J. P. et al., PrP expression and replication by Schwann cells: implications in prion spreading, J. Virol., 2002, 76, 2434–2439 Bremer J., Baumann F., Tiberi C., Wessig C., Fischer H., Schwarz P. et al., Axonal prion protein is required for peripheral myelin maintenance, Nat. Neurosci., 13, 310–318 Nazor K. E., Seward T., Telling G. C., Motor behavioral and neuropathological deficits in mice deficient for normal prion protein expression, Biochim. Biophys. Acta, 2007, 1772, 645–653 Arruda-Carvalho M., Njaine B., Silveira M. S., Linden R., Chiarini L. B., Hop/STI1 modulates retinal proliferation and cell death independent of PrPC, Biochem. Biophys. Res. Commun., 2007, 361, 474–480 Prinz M., Montrasio F., Furukawa H., van den Haar M. E., Schwarz P., Rülicke T. et al., Intrinsic resistance of oligodendrocytes to prion infection, J. Neurosci., 2004, 24, 5974–5981 Cohen R. I., Exploring oligodendrocyte guidance: ‘to boldly go where no cell has gone before’, Cell. Mol. Life Sci., 2005, 62, 505–510 Lappe-Siefke C., Goebbels S., Gravel M., Nicksch E., Lee J., Braun P. E. et al., Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination, Nat. Genet., 2003, 33, 366–374 Brück W., Inflammatory demyelination is not central to the pathogenesis of multiple sclerosis, J. Neurol., 2005, 252(Suppl. 5), v10–15 Chang A., Nishiyama A., Peterson J., Prineas J., Trapp B. D., NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions, J. Neurosci., 2000, 20, 6404–6412 Scolding N. J., Jones J., Compston D. A., Morgan B. P., Oligodendrocyte susceptibility to injury by T-cell perforin, Immunology, 1990, 70, 6–10 Russell J. H., Ley T. J., Lymphocyte-mediated cytotoxicity, Annu. Rev. Immunol., 2002, 20, 323–370 Antel J. P., Williams K., Blain M., McRea E., McLaurin J., Oligodendrocyte lysis by CD4+ T cells independent of tumor necrosis factor, Ann. Neurol., 1994, 35, 341–348 Baumann F., Tolnay M., Brabeck C., Pahnke J., Kloz U., Niemann H. H. et al., Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J., 2007, 26, 538–547 Hajj G. N., Lopes M. H., Mercadante A. F., Veiga S. S., da Silveira R. B., Santos T. G. et al., Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins, J. Cell Sci., 2007, 120, 1915–1926 Albrecht P. J., Murtie J. C., Ness J. K., Redwine J. M., Enterline J. R., Armstrong R. C. et al., Astrocytes produce CNTF during the remyelination phase of viral-induced spinal cord demyelination to stimulate FGF-2 production, Neurobiol. Dis., 2003, 13, 89–101 Brenneman D. E., Gozes I., A femtomolar-acting neuroprotective peptide, J. Clin. Invest., 1996, 97, 2299–2307 Gozes I., Bassan M., Zamostiano R., Pinhasov A., Davidson A., Giladi E. et al., A novel signaling molecule for neuropeptide action: activitydependent neuroprotective protein, Ann. N Y Acad. Sci., 1999, 897, 125–135 Volterra A., Meldolesi J., Astrocytes, from brain glue to communication elements: the revolution continues, Nat. Rev. Neurosci., 2005, 6, 626–640 Marin-Padilla M., Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: a Golgi study, J. Comp. Neurol., 1995, 357, 554–572 Liedtke W., Edelmann W., Bieri P. L., Chiu F. C., Cowan N. J., Kucherlapati R. et al., GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination, Neuron, 1996, 17, 607–615 Bartlett W. P., Knapp P. E., Skoff R. P., Glial conditioned medium enables jimpy oligodendrocytes to express properties of normal oligodendrocytes: production of myelin antigens and membranes, Glia, 1988, 1, 253–259 Gay F. W., Early cellular events in multiple sclerosis. Intimations of an extrinsic myelinolytic antigen, Clin. Neurol. Neurosurg., 2006, 108, 234–240 Matute C., Domercq M., Sanchez-Gomez M. V., Glutamate-mediated glial injury: mechanisms and clinical importance, Glia, 2006, 53, 212–224 Ambrosini E., Remoli M. E., Giacomini E., Rosicarelli B., Serafini B., Lande R. et al., Astrocytes produce dendritic cell-attracting chemokines in vitro and in multiple sclerosis lesions, J. Neuropathol. Exp. Neurol., 2005, 64, 706–715 Seifert G., Schilling K., Steinhauser C., Astrocyte dysfunction in neurological disorders: a molecular perspective, Nat. Rev. Neurosci., 2006, 7, 194–206 Bush T. G., Puvanachandra N., Horner C. H., Polito A., Ostenfeld T., Svendsen C. N. et al., Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice, Neuron, 1999, 23, 297–308 Berer K., Mues M., Koutrolos M., Rasbi Z. A., Boziki M., Johner C. et al., Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination, Nature, 2011, 479, 538–541 Olson J. K., Ludovic Croxford J., Miller S. D., Innate and adaptive immune requirements for induction of autoimmune demyelinating disease by molecular mimicry, Mol. Immunol., 2004, 40, 1103–1108 Noseworthy J. H., Progress in determining the causes and treatment of multiple sclerosis, Nature, 1999, 399(Suppl. 6738), A40–47 Haines J. L., Bradford Y., Garcia M. E., Reed A. D., Neumeister E., Pericak-Vance M. A. et al., Multiple susceptibility loci for multiple sclerosis, Hum. Mol. Genet., 2002, 11, 2251–2256 Lincoln M. R., Montpetit A., Cader M. Z., Saarela J., Dyment D. A., Tiislar M. et al., A predominant role for the HLA class II region in the association of the MHC region with multiple sclerosis, Nat. Genet., 2005, 37, 1108–1112 Kenealy S. J., Herrel L. A., Bradford Y., Schnetz-Boutaud N., Oksenberg J. R., Hauser S. L. et al., Examination of seven candidate regions for multiple sclerosis: strong evidence of linkage to chromosome 1q44, Genes Immun., 2006, 7, 73–76 Vandenbroeck K., Fiten P., Heggarty S., Goris A., Cocco E., Hawkins S. A. et al., Chromosome 7q21-22 and multiple sclerosis: evidence for a genetic susceptibility effect in vicinity to the protachykinin-1 gene, J. Neuroimmunol., 2002, 125, 141–148 Palma C., Minghetti L., Astolfi M., Ambrosini E., Silberstein F. C., Manzini S. et al., Functional characterization of substance P receptors on cultured human spinal cord astrocytes: synergism of substance P with cytokines in inducing interleukin-6 and prostaglandin E2 production, Glia, 1997, 21, 183–193 Lieb K., Fiebich B. L., Berger M., Bauer J., Schulze-Osthoff K., The neuropeptide substance P activates transcription factor NF-kappa B and kappa B-dependent gene expression in human astrocytoma cells, J. Immunol., 1997, 159, 4952–4958 Fiebich B. L., Schleicher S., Butcher R. D., Craig A., Lieb K., The neuropeptide substance P activates p38 mitogen-activated protein kinase resulting in IL-6 expression independently from NF-kappa B, J. Immunol., 2000, 165, 5606–5611 Antony J. M., van Marle G., Opii W., Butterfield D. A., Mallet F., Yong V. W. et al., Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination, Nat. Neurosci., 2004, 7, 1088–1095 Stuve O., Wang J., Chan A., Hemmer B., Cepok S., Nessler S. et al., No association between genetic polymorphism at codon 129 of the prion protein gene and primary progressive multiple sclerosis, Arch. Neurol., 68, 264–265 Stuve O., Korth C., Gabatto P., Cameron E. M., Hu W., Eagar T. N. et al., Genetic polymorphism at codon 129 of the prion protein gene is not associated with multiple sclerosis, Arch. Neurol., 2009, 66, 280–281 Rutishauser D., Mertz K. D., Moos R., Brunner E., Rülicke T., Calella A. M. et al., The comprehensive native interactome of a fully functional tagged prion protein, PLoS One, 2009, 4, e4446